Climate Change and Plant Pathosystems – Future Disease

Forum

Commentary Blackwell Publishing Ltd.

infestans, the causal agent of late blight of potato). We have Climate change and plant also seen disease alter the ecological landscape of a countr y pathosystems – future (e.g. chestnut blight, caused b y the fungus Cryphonectria (Endothia) parasitica). H istory tells us that w e can expect disease prevention starts plant disease to have devastating effects in the future. Plant diseases continue to destr oy crops and reduce agro- here nomic productivity – each year billions of dollars in yield are lost to diseases and millions mor e are spent managing these pests (Agrios, 1988). However, we now understand many of

The concentration of carbon dio xide (CO 2) in the the underlying principles surr ounding plant diseases, their atmosphere is incr easing (K eeling et al., 1989) and may epidemiology, and management (F ry, 1982). We know that double during this century (Bolin, 1986). The opportunities differing disease-causing organisms r equire differing envi- available for those inter ested in the study of plant diseases ronmental conditions for pathogenesis. We have mapped the within the emerging field of global change science w ere minimum, maximum, and optimum temperatur es and noted over a decade ago (B ruck & S hafer, 1991). However, moisture conditions for many pathogenic micr obes. We have the manner in which incr easing levels of atmospheric CO 2 also devised a variety of means for managing these organisms will affect cr op diseases r emains vir tually unstudied. O ne to r educe their impacts, including integration of cultural, group which has taken up this challenge and has begun to chemical and biological control strategies. We have observed address the effects of climate change and elev ated for many y ears that some plants r emain disease-free, while atmospheric CO2 on plant diseases is Sukumar Chakraborty their neighbors become infected or die. These early observa- and colleagues in Queensland, Australia. In this issue of New tions hav e led to strategies for br eeding cr ops which ar e Phytologist (pp. 733 –742), Chakrabor ty & D atta pr esent resistant to infection and, with ne w advances in biotechno- results fr om an indepth inv estigation of the effects of logical methodologies (Bent, 2003), host plant genetics remains elevated atmospheric CO 2 on a cr op, Stylosanthes scabra, to a primary weapon in our arsenal against plant disease. one of its major diseases (anthracnose, caused b y the fungus Colletotrichum gloeosporioides). Changing climate, changing research priorities We cannot continue to r ely on what w e know now, as our current global environment is changing. Increases in atmospheric ‘Climate change will directly impact crops, as well as concentrations of greenhouse gases has brought about concern for rising temperatures, altered precipitation patterns, as well their interactions with microbial pests’ as numerous other potential changes in our global climate (Norby et al., 2001; Paul, 2001). Climate change will directly impact crops, as well as their interactions with micr obial pests (Rosenzweig et al., 2000). While we can use current knowledge to predict how climatic changes might affect cr op productivity and interactions of crop plants with disease-causing organisms, few data are available to validate such speculations. This fact A glance at the past remains as true for the kno wn increase in atmospheric CO 2 Humans have been plagued b y the effects of plant diseases concentration as it does for potential increases in temperature since they first adopted an agrarian lifestyle, with the first or altered precipitation patterns. causes ascer tained and pr oven b y early scientists such as It is well established that elev ated CO 2 increases growth Tillet, Prevost, and de Bary (Ainsworth, 1981; Agrios, 1988). and yield of most plant species (Kimball, 1983) and that this We now kno w that numer ous types of micr oorganisms increase is generally caused b y increased rates of photosynthesis (primarily fungi, bacteria, nematodes, and vir uses) ar e the (Amthor, 1995) and/or incr eased water use efficiency (R ogers causal agents of diseases of both humans and plants. And w e & Dahlman, 1993). CO2-induced changes in plant morpho- have seen ho w plant disease has drastically alter ed histor y logy, physiology , and biochemistr y hav e the potential to (e.g. emigration fr om I reland in the mid 1800s r esulting effect the major diseases of the world ’s food and fiber cr ops. from the potato famine, due to the fungus Phytophthora Further, as with aspects of climate change, it has been

532 Forum Commentary

suggested that generalities r egarding effects of CO 2 on host– compounds and /or other changes in host physiology , pathogen interactions can be theoriz ed using kno wledge of morphology, or anatomy under elev ated CO 2 could lead to plant responses to elevated CO2 and of ecophysiological differ- reductions in incidence or severity, at least for some patho- ences among pathosystems (R union et al., 1994). H owever, systems (R union et al., 1994; H ibberd et al., 1996;

the manner in which increasing levels of atmospheric CO2 will Chakraborty et al., 2000; H artley et al., 2000). B y carrying affect crop diseases is only just beginning to be investigated. this pathosystem thr ough numer ous infection cy cles, the authors corr ectly note that enhanced r esistance at elev ated CO may not result in reduced host damage in the long term. What effects can elevated CO have on 2 2 Perhaps one of the most impor tant observations reported pathosystems? in this study, nevertheless following an earlier , similar ﬁnd- In this issue, Chakraborty & Datta present results from a study ing using the same pathosystem (Chakrabor ty et al., 2000), on the regionally important pasture legume Stylosanthes scabra. was an incr ease in fecundity (spor es pr oduced/lesion ar ea)

They investigated the effects of ambient and twice-ambient under elevated CO 2. This increase was noted for both iso- levels of atmospheric CO2 on changes in aggressiveness, fecun- lates but was mor e consistent and pr onounced for the mor e dity, and genotype of the fungal pathogen Colletotrichum aggressive of the two . Spore production has critical implica- gloeosporioides when grown for 25 successiv e infection cycles tions for the epidemiology of any disease – an incr ease in on host plant cultiv ars v arying in genetic r esistance to the spore numbers implies incr eased inoculum pressure for sub- disease. The findings are relevant not only to the genetics of sequent infection cy cles and, generally , an incr ease in the an impor tant host–pathogen interaction, but also to the spread and severity of disease. Although, through the inocu- epidemiology of this pathosystem. F irst, they demonstrate lation methods used, the authors ignor ed the effects of (using pathogen isolates collected fr om the field o ver the fecundity on aggressiveness and suggest the incr eased fecun- past 22 years) that, under field conditions, aggressiveness has dity was a result of a better canopy microclimate from larger

increased to wards the r esistant, but not the susceptible, plants under high CO 2, they nonetheless note that the high cultivar. It is inter esting to note that the authors ’ use of the reproductive fitness of the mor e aggr essive isolate is an term aggressiveness – which they define as a pr operty of the important component of its high lev el of aggr essiveness. fungus reflecting the relative amount of damage caused to the They fur ther note that incr eased fecundity under elev ated

host without regard to resistance genes – is synonymous with CO2 could hav e impor tant implications in the functional disease severity. Nonetheless, it seems logical that aggressiveness duration of resistance in crop plants. would not be alter ed on the susceptible cultiv ar as it can be Interestingly, while genotypic alterations occurred in both readily infected, placing little or no pr essure on the pathogen C. gloeosporioides isolates on the susceptible cultivar at twice-

for adaptation to sur vive and reproduce. However, disease sever- ambient CO2, they were not related to increased aggressive- ity (and pr esumably inoculum pr oduction) was substan- ness of the fungus. The authors duly note that: ther e ar e tially lower on the r esistant cultivar, ‘forcing’ the fungus to known mechanisms of genetic v ariation in this pathogen adapt by selecting for races which can infect this r esistant host. (i.e. hyper-v ariable chr omosomes and r etrotransposons, in The proportion of the overall population comprised by these addition to mutation and parasexual r ecombination); that races likely increased over time and resulted in increased severity. aggressiveness gr oups can arise fr om differing genetic line- The authors noted that aggr essiveness increased over the ages, can be inﬂuenced b y the physical envir onment, and course of the infection cy cles on both cultiv ars when grown may arise mor e frequently under w eather conditions fav or-

under ambient CO 2. They also note that this study is the able for pathogen growth; and therefore aggressiveness should ﬁrst to document a change in pathogen aggr essiveness when not necessarily be r elated to genetic alterations in the fun-

inoculated onto host plants and gr own under elevated CO2 gus. Still, it is curious that gr owth in elevated CO2 resulted – overall aggressiveness of both isolates was r educed on both in genetic alterations in both pathogen isolates only on the resistant and susceptible cultiv ars. This suggests that host susceptible cultiv ar, while this occurr ed only in ambient

plants may beneﬁt fr om futur e, higher atmospheric CO 2 CO2 for the more aggressive isolate on the r esistant cultivar. concentrations thr ough a r eduction in damage fr om this While the authors note that gr owth in elev ated CO 2 can pathogen. H owever, the o verall r eduction in pathogen result in numer ous changes in host morphology , anatomy, aggressiveness resulted from an initial lag phase of 10 infec- and physiology, speculation on possible factors driving the tion cycles, after which aggressiveness increased on both cul- more fr equently noted alterations in genotype under high

tivars. P resumably, during this initial period the pathogen CO2 would hav e been of inter est. I t is possible that an was adapting to whatev er CO2-induced changes in the host increase in host photosynthate pr oduction, providing a bet- led to the initial decr ease in aggr essiveness, after which ter substrate for fungal gr owth, r esulted in an incr ease in

aggressiveness incr eased in a manner similar to that which spore pr oduction under elev ated CO 2 (i.e. the incr ease in occurred on plants gr own under ambient CO 2. It has been fecundity noted), which r esulted in a mor e variable genetic suggested that an incr ease in pr oduction of defensiv e composition of the fungus. However, as the fecundity of the

Commentary Forum 533 more aggr essive isolate incr eased on the mor e r esistant Ainsworth GC. 1981. Introduction to the history of plant pathology. New York City, NY, USA: Cambridge University Press. cultivar under twice-ambient CO 2 (which did not exhibit any genetic alterations), this explanation appears not to fit Amthor JS. 1995. Terrestrial higher-plant response to increasing atmospheric [CO ] in relation to the global carbon cycle. Global the results obtained in this study. 2 Change Biology 1: 243–274. Bent AF. 2003. Crop diseases and strategies for their control. In: A look into the future Chrispeels MJ, Sadava DE, eds. Plants, genes, and crop biotechnology, 2nd edn. Sudbury, MA, USA: Jones and Bartlett Publishers, 391– Will disease incidence or sev erity incr ease, decr ease, or 413. remain essentially unchanged under future projected climate Bolin B. 1986. How much CO2 will remain in the atmosphere? and atmospheric composition conditions? This is a question In: Bolin B, Döös BR, Jäger J, Warrick RA, eds. The greenhouse of utmost impor tance to the futur e stability and security of effect, climatic change, and ecosystems. New York City, NY,USA: food and fiber pr oduction. Undoubtedly, rising temperatures, John Wiley & Sons, 93–155. Bruck RI, Shafer SR. 1991. A role for plant pathologists in global altered precipitation patterns, and increases in atmospheric CO 2 concentration will elicit complex changes in plant patho- climate change research. Plant Disease 75: 437. systems – these changes will vary depending on host responses, Chakraborty S, Data S. 2003. How will plant pathogens adapt to host plant resistance at elevated CO under a changing climate? New the pathosystem of inter est, and with the specific envir on- 2 Phytologist 159: 733–742. mental conditions in which they are grown. Although we can Chakraborty S, Pangga IB, Lupton J, Hart L, Room PM, Yates D. theorize that host–pathogen interactions might respond i n 2000. Production and dispersal of Colletotrichum gloeosporioides somewhat pr edictable ways, our curr ent lack of kno wledge spores on Stylosanthes scabra under elevated CO2. Environmental precludes having any r eal confidence in these pr edictions. Pollution 108: 381–387. Further, research on interacting effects of climatic v ariables Fry WE. 1982. Principles of plant disease management. New York City, with CO 2 have generally indicated that plant r esponses are NY, USA: Academic Press. complex, highly variable, and rarely follow predictable patterns. Hartley SE, Jones CG, Couper GC, Jones TH. 2000. Biosynthesis of plant phenolic compounds in elevated atmospheric CO . Global Nonetheless, we must begin some where as the CO 2 con- 2 centration in the atmosphere rises, will probably continue to Change Biology 6: 497–506. do so into the for eseeable futur e, and will likely elicit Hibberd JM, Whitbread R, Farrar JF. 1996. Effect of elevated concentrations of CO on infection of barley by Erysiphe graminis. changes in the global climate. N o definitiv e answ ers ar e 2 Physiological and Molecular Plant Pathology 48: 37–53. forthcoming from the curr ent study, nor should they hav e Keeling CD, Bacastow RB, Carter AF, Piper SC, Whorf TP, been expected – the question is too br oad and v ariable to Heimann M, Mook WG, Roeloffzen H. 1989. A three address in a single study . However, the study does pr ovide dimensional model of atmospheric CO2 transport based on evidence suggesting that: elev ated atmospheric CO 2 can observed winds: Observational data and preliminary analysis. impact impor tant cr op pathosystems; pathogen aggr essive- In: Peterson DH, ed. Aspects of climate variability in the pacific ness/disease severity might be decr eased under rising CO 2, and the Western Americas Geophysical Monograph 55. Washington which suggests ther e may be plant r esponses which can be DC, USA: The American Geophysical Union, 165–235. taken advantage of within br eeding programs; this decr ease Kimball BA. 1983. Carbon dioxide and agricultural yield: an in pathogen aggr essiveness may not hold in the long term; assemblage and analysis of 770 prior observations. USDA/ARS fecundity may incr ease, which implies farmers will likely Water Conservation Laboratory Report Number 14. Phoenix, AZ, need to alter disease management strategies; and pathogen USA: US Department of Agriculture, Agricultural Research Service. Norby RJ, Kobayashi K, Kimball BA. 2001. Rising CO – future evolution might be accelerated under a high CO environ- 2 2 ecosystems. New Phytologist 150: 215–221. ment. There are many more questions than there are answers. Paul N. 2001. Plant responses to UV-B: time to look beyond stratospheric ozone depletion? New Phytologist 150: 1–8. G. Brett Runion Rogers HH, Dahlman RC. 1993. Crop responses to CO2 enrichment. Vegetatio 104/105: 117–131. Plant Pathologist/Soil Microbiologist, Rosenzweig C, Iglesias A, Yang YB, Epstein PR, Chivian E. USDA-ARS, National Soil Dynamics Laboratory, 2000. Climate Change and U.S. Agriculture: The Impacts of 411 S. Donahue Drive, Warming and Extreme Weather Events on Productivity, Plant Auburn, AL 36832, USA Diseases and Pests. Boston, MA, USA: Center For Health and (tel +1334 8444517; fax +1334 8878597; the Global Environment, Harvard Medical School. email [email protected]) Runion GB, Curl EA, Rogers HH, Backman PA, Rodriguez-Kabana R, Helms BE. 1994. Effects of free-air CO2 enrichment on microbial populations in the rhizosphere and phyllosphere of cotton. References Agricultural and Forest Meteorology 70: 117–130.

Agrios GN. 1988. Plant pathology, 3rd edn. New York City, NY, USA: Key words: climate change, plant pathogen, Stylosanthes scabra, Academic Press. anthracnose, Colletotrichum gloeosporioides.