Enlarging upon this topic, Chakraborty and Datta (2003) report that "changes in plant physiology, anatomy and morphology that have been implicated in increased resistance or [that] can potentially enhance host resistance at elevated CO2 include: increased net photosynthesis allowing mobilization of resources into host resistance (Hibberd et al., 1996a.); reduced stomatal density and conductance (Hibberd et al., 1996b); greater accumulation of carbohydrates in leaves; more waxes, extra layers of epidermal cells and increased fibre content (Owensby, 1994); production of papillae and accumulation of silicon at penetration sites (Hibberd et al., 1996a); greater number of mesophyll cells (Bowes, 1993); and increased biosynthesis of phenolics (Hartley et al., 2000), among others."

Adding to this impressive list, Chakraborty and Datta elucidated yet another way in which atmospheric CO2 enrichment may tip the scales in favor of plants in a study of the aggressiveness of the fungal anthracnose pathogen Colletotrichum gloeosporioides, wherein they inoculated two isolates of the pathogen onto two cultivars of the tropical pasture legume Stylosanthes scabra (Fitzroy, which is susceptible to the fungal pathogen, and Seca, which is more resistant) over the course of 25 sequential infection cycles at ambient (350 ppm) and elevated (700 ppm) atmospheric CO2 concentrations in controlled environment chambers.  This protocol revealed that "at twice-ambient CO2 the overall level of aggressiveness of the two [pathogen] isolates was significantly reduced on both [host] cultivars."  In addition, they say that "as shown previously (Chakraborty et al., 2000), the susceptible Fitzroy develops a level of resistance to anthracnose at elevated CO2, but resistance in Seca remains largely unchanged."

Simultaneously, however, pathogen fecundity was found to increase at twice-ambient CO2.  Of this finding, they report that their results "concur with the handful of studies that have demonstrated increased pathogen fecundity at elevated CO2 (Hibberd et al., 1996a; Klironomos et al., 1997; Chakraborty et al., 2000)."  How this happened in the situation they investigated, as they describe it, is that the overall increase in fecundity at high CO2 "is a reflection of the altered canopy environment," wherein "the 30% larger S. scabra plants at high CO2 (Chakraborty et al., 2000) makes the canopy microclimate more conducive to anthracnose development."

In view of the opposing changes induced in pathogen behavior by elevated levels of atmospheric CO2 in this specific study - reduced aggressiveness but increased fecundity - it is difficult to know the ultimate outcome of atmospheric CO2 enrichment for the pathogen-host relationship.  More research, especially under realistic field conditions, will be needed to clarify the situation; and, of course, different results are likely to be observed for different pathogen-host associations.  What is more, results could also differ under different climatic conditions.  Nevertheless, the large number of ways in which elevated CO2 has been demonstrated to increase plant resistance to pathogen attack suggests that plants may well gain the advantage over pathogens as the air's CO2 content continues to climb in the years ahead; and in the paragraphs that follow, we review the results of a number of studies that support this assessment of the issue.

Malmstrom and Field (1997) grew individual oat plants for two months in pots within phytocells maintained at CO2 concentrations of 350 and 700 ppm, while a third of each CO2 treatment's plants were infected with the barley yellow dwarf virus (BYDV), which plagues more than 150 plant species worldwide, including all major cereal crops.  They found that the elevated CO2 stimulated net photosynthesis rates in all plants, but with the greatest increase occurring in diseased individuals (48% vs. 34%).  In addition, atmospheric CO2 enrichment decreased stomatal conductance by 34% in healthy plants, but by 50% in infected ones, thus reducing transpirational water losses more in infected plants.  Together, these two phenomena contributed to a CO2-induced doubling of the instantaneous water-use efficiency of healthy control plants, but to a much larger 2.7-fold increase in diseased plants.  Thus, although BYDV infection did indeed reduce overall plant biomass production, the growth response to elevated CO2 was greatest in the diseased plants.  After 60 days of CO2 enrichment, for example, total plant biomass increased by 36% in infected plants, while it increased by only 12% in healthy plants.  In addition, while elevated CO2 had little effect on root growth in healthy plants, it increased root biomass in infected plants by up to 60%.  In their concluding remarks, therefore, Malmstrom and Field say that CO2 enrichment "may reduce losses of infected plants to drought" and "may enable diseased plants to compete better with healthy neighbors."

Tiedemann and Firsching (2000) grew spring wheat from germination to maturity in controlled environment chambers maintained at either ambient (377 ppm) or enriched (612 ppm) atmospheric CO2 concentrations and either ambient (20 ppb) or enriched (61 ppb) atmospheric ozone (O3) concentrations, while half of the plants in each of the four resulting treatments were inoculated with a leaf rust-causing pathogen.  These procedures revealed that the percent of leaf area infected by rust in inoculated plants was largely unaffected by atmospheric CO2 enrichment but strongly reduced by elevated O3.  With respect to photosynthesis, elevated CO2 increased rates in inoculated plants by 20 and 42% at ambient and elevated O3 concentrations, respectively.  Although inoculated plants produced lower yields than non-inoculated plants, atmospheric CO2 enrichment still stimulated yield in infected plants, increasing it by fully 57% at high O3.  Consequently, the beneficial effects of elevated CO2 on wheat photosynthesis and yield continue to be expressed in the presence of both O3 and pathogenic stresses.

In another joint CO2/O3 study, 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.

Jwa and Walling (2001) grew tomato plants in hydroponic culture for eight weeks in controlled environment chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm.  At week five of their study, half of the plants growing in each CO2 concentration were infected with the fungal pathogen Phytophthora parasitica, which attacks plant roots and induces water stress that ultimately decreases plant growth and yield.  This infection procedure ultimately reduced total plant biomass by nearly 30% at both atmospheric CO2 concentrations.  However, the elevated CO2 treatment increased the total biomass of healthy and infected plants by the same percentage, so that infected tomato plants grown at 700 ppm CO2 exhibited biomass values similar to those of healthy tomato plants grown at 350 ppm CO2.  Consequently, atmospheric CO2 enrichment completely counterbalanced the negative effects of Phytophthora parasitica infection on tomato productivity.

Pangga et al. (2004) grew well-watered and fertilized pencilflower (cultivar Fitzroy) seedlings - an important legume crop susceptible to anthracnose disease caused by Colletotrichum gloeosporioides - within a controlled environment facility maintained at atmospheric CO2 concentrations of either 350 or 700 ppm, where they inoculated six-, nine- and twelve-week-old plants with conidia of C. gloeosporioides.  Then, ten days after inoculation, they counted the anthracnose lesions on the plants and classified them as either resistant or susceptible.  In doing so, they found that "the mean number of susceptible, resistant, and total lesions per leaf averaged over the three plant ages was significantly (P<0.05) greater at 350 ppm than at 700 ppm CO2, reflecting the development of a level of resistance in susceptible cv. Fitzroy at high CO2."  In fact, with respect to plants inoculated at twelve weeks of age, they say that those grown "at 350 ppm had 60 and 75% more susceptible and resistant lesions per leaf, respectively, than those [grown] at 700 ppm CO2."  Last of all, the Australian scientists say their work "clearly shows that at 350 ppm overall susceptibility of the canopy increases with increasing age because more young leaves are produced on secondary and tertiary branches of the more advanced plants."  However, they report that "at 700 ppm CO2, infection efficiency did not increase with increasing plant age despite the presence of many more young leaves in the enlarged canopy," which finding, in their words, "points to reduced pathogen efficiency or an induced partial resistance to anthracnose in Fitzroy at 700 ppm CO2."

In conclusion, the balance of evidence obtained to date appears to demonstrate an enhanced ability of plants to withstand pathogen attacks in CO2-enriched as opposed to ambient-CO2 air.  Hence, as the atmosphere's CO2 concentration continues to rise 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.

References
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Chakraborty, S. and Datta, S.  2003.  How will plant pathogens adapt to host plant resistance at elevated CO2 under a changing climate?  New Phytologist 159: 733-742.

Chakraborty, S., Pangga, I.B., Lupton, J., Hart, L., Room, P.M. and Yates, D.  2000.  Production and dispersal of Colletotrichum gloeosporioides spores on Stylosanthes scabra under elevated CO2.  Environmental Pollution 108: 381-387.

Hartley, S.E., Jones, C.G. and Couper, G.C.  2000.  Biosynthesis of plant phenolic compounds in elevated atmospheric CO2.  Global Change Biology 6: 497-506.

Hibberd, J.M., Whitbread, R. and Farrar, J.F.  1996a.  Effect of elevated concentrations of CO2 on infection of barley by Erysiphe graminis.  Physiological and Molecular Plant Pathology 48: 37-53.

Hibberd, J.M., Whitbread, R. and Farrar, J.F.  1996b.  Effect of 700 µmol per mol CO2 and infection of powdery mildew on the growth and partitioning of barley.  New Phytologist 134: 309-345.

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Malmstrom, C.M. and Field, C.B.  1997.  Virus-induced differences in the response of oat plants to elevated carbon dioxide.  Plant, Cell and Environment 20: 178-188.

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Pangga, I.B., Chakraborty, S. and Yates, D.  2004.  Canopy size and induced resistance in Stylosanthes scabra determine anthracnose severity at high CO2.  Phytopathology 94: 221-227.

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Tiedemann, A.V. and Firsching, K.H.  2000.  Interactive effects of elevated ozone and carbon dioxide on growth and yield of leaf rust-infected versus non-infected wheat.  Environmental Pollution 108: 357-363.