Introduction

Climate change is the realist now and biggest threat of the present century. Climate change is affecting plants in natural and agricultural ecosystems throughout the world (Stern 2007). It is already contributing to the death of nearly 400,000 people a year and costing the world more than US$ 1.2 trillion, thus wiping 1.6% annually from the global GDP (McKinnon, 2012). Climate change is the result of the acceleration in the increase in temperature and CO2 concentration over the last 100 years. During the period, the global mean temperature has increased by 0.74°C and atmospheric CO2 concentration has increased from 280 ppm in 1750 to 400 ppm in 2013. It is widely accepted that human activities are now increasingly influencing changes in global climate (Reisinger & Pachauri 2007). The impact of climate change has been observed in many dimensions such as effects on biodiversity, food grain production, insects and plant diseases. Out of this, impact on plant diseases is also a one of the important dimension that has to be seen in broader prospective. Plant pathogens are ubiquitous in natural and managed systems, being among the first to demonstrate the effects of climate change due to the numerous populations, ease of reproduction and dispersal, and short time between generations. Therefore, they constitute a fundamental group of biological indicators that needs to be evaluated regarding climate change impacts, besides being responsible for production losses, and potentially threat to agro-ecosystem sustainability. Since plant diseases are a significant constraint to the production of some 25 crops that stand between the rapidly expanding world population and starvation. Changes in environmental conditions are strongly associated with differences in the level of losses caused by a disease because the environment significantly (directly or indirectly) influences plants, pathogens and their antagonists. The changes associated with global warming (i.e., increased temperatures, changes in the quantity and pattern of precipitation, increased CO2 and ozone levels, drought, etc.) thus, may affect the incidence and severity of plant disease and influence the further co-evolution of plants and their pathogens (Eastburn et al., 2011). Anthropogenic activities have also been found to contribute to the spread of many diseases like sudden oak death (Prospero et al., 2009). Climate change directly impacts crops, as well as their interactions with microbial pests (Rosenzweig et al., 2000). However, little work has been done to model the effects of climate change on plant disease epidemics (Garrett et al., 2006). Changing weather can induce severe plant disease epidemics, which threaten food security if they affect staple crops and can damage landscapes if they affect amenity species. This article focused on impacts of climate change on the spatial and temporal distribution of plant diseases, the effects of increased concentration of atmospheric CO2 and the consequences for disease control.

Impact of climate change on plant patho-systems

Plant diseases play an important role in agriculture. But at present very limited information on the potential impacts of climate change on plant diseases is available. The role of environment is well known since long back: the classic disease triangle emphasizes the interactions between plant hosts, pathogens and environment in causing disease (Grulke, 2011).

Climate change is just one of the many ways in which the environment can move in the long term from disease-suppressive to disease-conducive or vice versa. Therefore, plant diseases could be even used as indicators of climate change, although there may be other bio-indicators which are easier to monitor. Long-term datasets on plant disease development under changing environmental conditions are rare, but, when available, can demonstrate the key importance of environmental change for plant health . Plant health is predicted to generally suffer under climate change through a variety of mechanisms, from accelerated pathogen evolution and shorter incubation periods to enhanced abiotic stress due to mismatches between ecosystems and their climate and the more frequent occurrence of extreme weather events. Drought is expected to lead to increased frequency of tree pathogens, mainly through indirect effects on host physiology. Drier conditions may also have direct effects on pathogens, as shown by the invasive exotic species Heterobasidion irregulare in central Italy, which appears better adapted to dispersal in the Mediterranean climate than the native H. annosum species. Conversely, for pathogens that take advantage of frost-wounds in order to infect the host (e.g. Seiridium cardinale on cypress species), a decreased occurrence of frost could lead to reduction in disease incidence. In the case of insect-vectored diseases: if warmer temperatures translate into additional insect generations, obviously this will increase transmission rates of the invasive pathogen (Robinet et al., 2011).

Impact of climate change on geographical and temporal distribution of plant pathogens:

Since environment and diseases are closely related, climate change will probably alter the geographical and temporal distribution of phyto-sanitary problems. The host plant agro-climatic zoning for coffee will be altered, as showed by Assad et al. (2004); likewise, pathogens and other microorganisms related to the disease process will be affected.

Therefore, new diseases may arise in certain regions, and other diseases may cease to be economically important, especially if the host plant migrates into new areas (Coakley et al., 1999). According to them, pathogens tend to follow the host plant in its geographical distribution, but the rate at which pathogens become established in the new environment is a function of the mechanism of pathogen dispersal, suitability of the environment for dispersal, survival between seasons, and physiological and ecological changes in the host plant. According to Chakraborty et al. (2000a), more aggressive strains of pathogen with broad host range, such as Rhizoctonia, Sclerotinia, Sclerotium and other necrotrophic pathogens can migrate from agro-ecosystems to natural vegetation and less aggressive pathogens from natural plant communities can start causing damage in monocultures of nearby regions. Regarding unspecialized necrotrophs, the range of hosts can be extended due to crop migration. For vector-transmitted pathogens the risk analysis may include the effects of climate change on the vector population, as discussed by Harrington (2002) for the barley yellow dwarf disease.

Impact of changes in temperature on pathogens and disease

Change in temperature will directly influence infection, reproduction, dispersal, and survival between seasons and other critical stages in the life cycle of a pathogen.

• At higher temperature, lignification of cell walls increased in forage species and enhanced resistance to fungal pathogens. Impact would, therefore, depend on the nature of the host- pathogen interactions and mechanism of resistance.

• Increase in temperature with sufficient soil moisture may increase evapo-transpiration resulting in humid microclimate in crop canopy and may lead to incidence of diseases favoured under warm and humid conditions.

• Some of the soil-borne diseases may increase at the rise of soil temperature. If climate change causes a gradual shift of cropping regions, pathogens will follow their host. Analysis of long-term data of wheat and rice diseases in China has shown trends of an increase in minimum temperatures in association with the abundance of rice blast or wheat scab.

• In most locations, temperature changes had significant effects on disease development. However, these effects varied between different agro-ecological zones. In cool sub-tropical zones such as Japan and northern China, elevation of ambient temperature resulted in greater risk of blast epidemics.

• Situations in the humid tropics and warm humid subtropics were opposite to those in cool areas. A lower temperature resulted in greater risk of blast epidemics.

Examples of effect of climate change on crop production

1. In rice with rise temperature symptoms of brown spot and narrow brown leaf spot seen in farmers’ fields in West and East Africa which were never seen earlier.

2. Wheat and oats become more susceptible to rust diseases with increased temperature; but some forage species become more resistant to fungi with increased temperature

3. Temperate climate zones that include seasons with cold average temperatures are likely to experience longer periods of temperatures suitable for pathogen growth and reproduction if climates warm. For example, predictive models for potato and tomato late blight (caused by Phytophthora infestans) show that the fungus infects and reproduces most successfully during periods of high moisture that occur when temperatures are between 45o F (7.2 o C) and 80 o F (26.8 o C)

4. Temperature is one of the most important factors affecting the occurrence of bacterial diseases such as Ralstonia solanacearum, Acidovorax avenae and Burkholderia glumea. Thus, bacteria could proliferate in areas where temperature-dependent diseases have not been previously observed.

5. The increased mean winter temperatures, the shift in precipitation from summer to winter and the tendency toward heavier rain, which have been noted in central Europe, favour infection by several Phytophthora species and thus increased incidence of root rot in forest trees. For example, in the southern United Kingdom, recent climatic changes have affected the geographical range and severity of phoma stem canker (Leptosphaeria maculans) of oilseed rape (Brassica napus).

6. Genetic changes in the virus through mutation and recombination, changes in the vector populations and long-distance transportation of plant material or vector insects due to trade of vegetables and ornamental plants have resulted in the emergence of tomato yellow leaf curl disease, African cassava mosaic disease, diseases caused by bipartite begomoviruses in Latin America, Ipomovirus diseases of cucurbits, tomato chlorosis caused by criniviruses, and the torrado-like diseases of tomato.

7. Temperature can also affect disease resistance in plants, thus affecting the incidence and severity of the diseases. Temperature sensitivity to resistance has been reported for leaf rust (Puccinia recondita) in wheat, broomrape (Orobanche cumana) in sunflower, black
shank (Phytophthora nicotianae) in tobacco and bacterial blight (Xanthomonas oryzae pv. oryzae) in rice.

8. Incidence of yellow rust, powdery mildew, leaf spot blotch/blight, covered smut, loose smut, foot/root rot and cereal cyst nematode causing molya disease were encountered at cold arid trans-Himalayan Ladakh region of India bordering with Pakistan and China.

9. Due to high temperature oil palms (OP) are subjected to fungal diseases of which Fusarium wilt and Ganoderma rots are the most important.

Impact of changes in moisture on pathogens and disease

Moisture is particularly important to pathogenic bacteria and fungi. The rain duration necessary for infection varies with temperature. Usually, a longer period of leaf wetness is needed to establish an infection in cooler temperatures, as germination and infection are generally accelerated in warmer conditions.

• Some pathogens such as apple scab, late blight, and several vegetable root pathogens are more likely to infect plants with increased moisture â€" forecast models for these diseases are based on leaf wetness, relative humidity and precipitation measurements.

• Other pathogens like the powdery mildew species tend to thrive in conditions with lower (but not low) moisture.

• More frequent and extreme precipitation events that are predicted by some climate change models could result in more and longer periods with favorable pathogen environments.

• Host crops with canopy size limited by lack of moisture might no longer be so limited and may produce canopies that hold moisture in the form of leaf wetness or high canopy relative humidity for longer periods, thus increasing the risk from pathogen infection.

• Some climate change models predict higher atmospheric water vapor concentrations with increased temperature â€" this also would favor pathogen and disease development.


Impact of rising CO2 levels on pathogens and disease

Increased CO2 levels can impact both the host and the pathogen in multiple ways.

1. Decomposition of plant litter is important for nutrient cycling and in the saprophytic survival of many pathogens. Because of high C: N ratio of litter as a consequence of plant growth under elevated CO2, decomposition will be slower. Increased plant biomass, slower decomposition of litter, and higher winter temperature could increase pathogen survival on over-wintering crop residues and increase the amount of initial inoculation available for subsequent infection.

2. Some fungal pathosystems under elevated CO2 revealed two important trends. First, delay in the initial establishment of the pathogen because of modifications in pathogen aggressiveness and/or host susceptibility. For example, reduction in the rate of primary penetration of Eysiphe graminis on barley and a lengthening of latent period in Maravalia cryptostegiae (rubervine rust) has been observed under elevated CO2. Here, host resistance may have increased because of change in host morphology, physiology, nutrients and water balance. A decrease in stomatal density increases resistance to pathogens that penetrate through stomata. Under elevated CO2 barley plants were able to mobilize assimilates into defense structures including the formation of papillae and accumulation of silicon at sites of appressorial penetration of Erysiphe graminis.

3. At elevated CO2, increased partitioning of assimilates to roots occurs consistently in crops such as carrot, sugar beet, and radish. If more carbon is stored in roots, losses from soil-borne diseases of root crops may be reduced under climate change. In contrast, for foliage diseases favored by high temperature and humidity, increases in temperature and precipitation under climate change may result in increased crop loss. The effects of enlarged plant canopies from elevated CO2 could further increase crop losses from foliar pathogens.

4. The second important effect is an increase in the fecundity of pathogens under elevated CO2 following penetration, established colonies of Erysiphe graminisgrew faster and sporulation per unit area of infected tissue was increased several-fold under elevated CO2. It has been also observed that under elevated CO2out of the 10 biotrophic pathogens studied, disease severity was enhanced in six and reduced in four and out of 15 necrotrophic pathogens, disease severity increased in nine, reduced in four and remained unchanged in the other two.

Elevated levels of atmospheric pollutants (ozone and nitrous oxide)

Exposure to 5-10 ppm ozone for a few hours can cause visible injury to sensitive crops like barley, tomato, onion, potato, soybean, tobacco, and wheat. Plants appear to be less sensitive to nitrous oxide, however, higher concentrations can cause water-soaked lesions, which soon turn brown. Ozone and nitrous oxide injury on plants in turn may add new problem to pathologists in diagnosis. Current climate change scenarios predict a further increase of tropospheric ozone, which is well known to inhibit plant photosynthesis and growth process. Ozone can also predispose plants to enhanced biotic attack, as proposed in particular for necrotrophic fungi, root rot fungi and black beetles. Onions injured by ozone exposure were more susceptible to Botrytis cinerea, but not to B. squamosa. Increased onion yields and reduced dieback when filters removed ambient ozone has been also observed in some experimental studies.

Impact of acid rain

Most studies on the effect of acid rain were done with simulated acid rain since it is not easy to establish experiments under field conditions. In first year of experiment no effect of acid rain has been observed on any of four pathosystems: alfalfa leaf spot, peanut leaf spot (PLS), potato late blight (PLB), and soybean brown spot. In the second year, PLS severity decreased with increasing acidity and the dose response was linear; PLB severity showed a curvilinear response to acid rain.

Elevated ultraviolet B

Studies indicate that the UV-B component of solar radiation plays a natural regulation on plant diseases. Stimulatory effect of near-UV light on reproduction of many fungi, and spore production in Leptosphaerulina trifoli peaks at 287 nm are reported. Fungi differ in their sensitivity to UV-B. Some strains of Septoria tritici are more sensitive to UV-B than others and S. nodorum, as a species, is more sensitive than S. tritici. UV-B radiation can modify the relative composition of phylloplane organisms, such as pink and white yeast. Continued exposure to enhanced UV-B radiation lowers the level of antifungal compounds in foliar parts. UV-B has been shown to reduce tolerance of rice to blast (Pyricularia grisea) and although higher UV-B reduced plant biomass and leaf area; there was no increase in blast severity..

Effects of climate change on viral pathogens

Tobacco plants grown at increased CO2concentrations showed a markedly decreased spread of virus. It appears that CO2 rise in the air may have some positive effects, which may likely offset the negative effects of virus infection. However, generalization is difficult without much information from different virus-host infections. Most plant viruses are transmitted by vectors and majority by insects. Particularly aphids are expected to react strongly to environmental changes because of their short generation time, low developmental threshold temperatures and ability to survive mild winters without winter storms. An increase in the number of insect vectors will inevitably lead to a higher risk for viral infection of plants. The aphid transmissible complex of barley yellow dwarf viruses in cereals and potato virus Y in potato are amenable to show potential effects on the prevalence of infection because of climate change.

Therefore, with predicted changes in climate, viral diseases of plants are expected to increase in importance. Potentially of greater importance will be the effects of diseases caused by newly, introduced viruses that, because of the changed climate, will be able to persist. A warmer climate might also allow viruses that are present in greenhouses, such as Pepino mosaic virus (PepMV), to establish infection in the field. The main effect of temperature in temperate regions is to influence winter survival of vectors. Natural spread of vectors, pests and diseases is accelerated towards the North, as former climate barriers are no longer effective. This results in more severe outbreaks of plant-disease vectors like aphids, white flies, thrips or beetles, an extension of the period of disease infection further into the growing season and also introduction and establishment of new vector species. The described effects on vectors can have severe negative effects on food production or result in an increased use of plant protection products to control the vectors.

Effects of climate change on bacterial pathogens

Host or debris-borne bacteria survive on and in host tissues. On perennial hosts, bacteria, such as Erwinia amylovora on apple, overwinter on infected host tissue, and primary inoculum is spread from host to host in the next season. On annual hosts, bacteria such as Pseudomonas syringae pv. phaseolicola may survive in host debris in soil or on the soil surface. Vector-borne bacterial pathogens, such as Erwinia stewartii, survive in insect vectors, and these vectors act as the source of primary inoculum in the next season. Bacterial pathogens, such as Pseudomonas syringae pv. tomato and Xanthomonas campestris pv. vesicatoria, arise from infected seed and possibly also survive in debris, soil, and weeds. Bacteria are spread to their host plants mainly by water, usually in the form of rain splash, and insects. In humid, wet conditions, infected plant tissues can exude masses of bacteria that are spread from host to host by rain splash and insects. Therefore, the warmer drier summers expected with climate change should limit bacterial diseases. However, bacteria often enter hosts through wounds and the expected increase in frequency and intensity of summer storms with high winds, rain, and hail will increase wounding of plants and provide moisture for the spread of bacteria.

Effects of climate change on nematodes

Majority of plant-pathogenic nematodes spend part of their lives in soil, and therefore, soil is the source of primary inoculum. Life cycle of a nematode can be completed within 2â€"4 weeks under optimum environmental conditions. Temperature is the most important factor, and development is slower with cooler soil temperatures. Warmer soil temperatures are expected to accelerate nematode development, perhaps resulting in additional generations per season, and drier temperatures are expected to increase symptoms of water stress in plants infected with nematodes such as the soybean cyst nematode. Overwintering of nematodes is not expected to be significantly affected by changes in climate, although for some, such as the soybean cyst nematode, egg viability may be reduced in mild winters.

Effects of climate change on disease development due to abiotic stresses

Diseases can also result from indirect effects, where plants have their defences weakened by an abiotic factor and are predisposed to infection by plant pathogens. Several important plant diseases are initiated by abiotic stresses, including forest decline diseases, which are an example of a disease complex caused by a combination of plant predisposition and a repetitive sequence of plant stresses that weaken a plant to become susceptible to weak pathogens that then can often infect and kill the plant These weak pathogens, called saprogens, are often ubiquitous inhabitants of soil and decaying plant material and, normally, they do not cause disease in healthy, unstressed plants. However, under conditions of environmental stress, plants can become susceptible to these saprogens and their opportunistic infections. One of the more prevalent examples of these saprogens is the girdling fungi of the genus Armillaria. As climate changes, new combinations of hostâ€"stressâ€"saprogens will be encountered and might give rise to new types of decline diseases, particularly in tree species. In particular, forest declines are an example of plant diseases that result from a combination of interacting biotic and abiotic factors. Such diseases are characterized by a variety of disease symptoms and signs, are typically scattered in a random pattern throughout a population within a region, and are often host-specific, although more than one tree species in a region may have its own specific decline symptoms. Decline diseases are one example where a strong association between climate change and disease incidence and (or) severity has already been established in several forest species.

Impact of climate change on disease management practices

Pathogen modifies host resistance, and result in changes in the physiology of host-pathogen interactions. The most likely consequences are shifts in the geographical distribution of host and pathogen and altered crop losses, caused in part by changes in the efficacy of control strategies (Coakley et al., 1999). While physiological changes in host plants may result in higher disease resistance under climate change scenarios, host resistance to disease may be overcome more quickly by more rapid disease cycles, resulting in a greater chance of pathogens evolving to overcome host plant resistance. Fungicide and bactericide efficacy may change with increased CO2, moisture, and temperature. The more frequent rainfall events predicted by climate change models could result in farmers finding it difficult to keep residues of contact fungicides on plants, triggering more frequent applications. Systemic fungicides could be affected negatively by physiological changes that slow uptake rates, such as smaller stomatal opening or thicker epicuticular waxes in crop plants grown under higher temperatures. These same fungicides could be affected positively by increased plant metabolic rates that could increase fungicide uptake. It is not well understood how naturally-occurring biological control of pathogens by other microbial organisms could change as populations of microorganisms shift under changed temperature and moisture regimes â€" in some cases antagonistic organisms may out-compete pathogens while in others pathogens may be favored. Exclusion of pathogens and quarantines through regulatory means may become more difficult for authorities as unexpected pathogens might appear more frequently on imported crops.

Need for adoption of novel approaches

Changing disease scenario due to climate change has highlighted the need for better agricultural practices and use of eco-friendly methods in disease management for sustainable crop production. In the changing climate and shift in seasons, choice of crop management practices based on the prevailing situation is important. In such scenarios, weather-based disease monitoring, inoculums monitoring, especially for soil-borne diseases and rapid diagnostics would play a significant role. There is need to adopt novel approaches to counter the resurgence of diseases under changed climatic scenario. Integrated disease management strategies should be developed to decrease dependence on fungicides. Other multipronged approaches include healthy seeds with innate forms of broad and durable disease resistance, and intercropping systems that foster refuges for natural biocontrol organisms. In addition, monitoring and early warning systems for forecasting disease epidemics should be developed for important hostâ€"pathogens which have a direct bearing on the earnings of the farmers and food security at large. Such as diversified crop protection strategy has been highlighted in a comprehensive study on an integrated approach to control all foliar diseases in barley. Use of botanical pesticides and plant-derived soil amendments such as neem oil, neem cake and karanja seed extract also help in mitigation of climate change because it helps in the reduction of nitrous oxide emission by nitrification inhibitors such as nitrapyrin and dicyandiamide.

Conclusions

Understanding the potential effects of climate change on agriculture in terms of its impacts on severity and incidence of pests and diseases is an important issue. Climate changes will affect diseases, yield and quality of crops. Our knowledge is limited on how multifactor climate changes may affect plant health. The prediction is that climate change may alter rates of pathogen development, modify host resistance and lead to changes in the physiology of host - pathogen interactions, which again may influence the severity of plant diseases. Climate change can have positive, negative, or neutral impact on individual pathosystems because of the specific nature of the interactions of host and pathogen. Climate change operates at a global scale; a lack of understanding of epidemic processes at relevant environmental and spatial scales has hampered progress. From a disease management viewpoint, information is generally required for a specific disease at a field scale; hence, data on potential impacts of climate change need to be assessed and evaluated at a detailed level to capture important mechanisms and dynamics that drive epidemics.

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