S. Chakraborty

CLIMATE CHANGE AND PLANT DISEASE MANAGEMENT

▪ Abstract  Research on impacts of climate change on plant diseases has been limited, with most work concentrating on the effects of a single atmospheric constituent or meteorological variable on the host, pathogen, or the interaction of the two under controlled conditions. Results indicate that climate change could alter stages and rates of development of the pathogen, modify 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. Recent developments in experimental and modeling techniques offer considerable promise for developing an improved capability for climate change impact assessment and mitigation. Compared with major technological, environmental, and socioeconomic changes affecting agricultural production during the next century, climate change may be less important; it will, however, add another layer of complexity and uncertainty onto a system that is already exceedingly difficult to manage on a sustainable basis. Intensified research on climate change-related issues could result in improved understanding and management of plant diseases in the face of current and future climate extremes.

Climate change: potential impact on plant diseases

Global climate has changed since pre-industrial times. Atmospheric CO(2), a major greenhouse gas, has increased by nearly 30% and temperature has risen by 0.3 to 0.6 degrees C. The intergovernmental panel on climate change predicts that with the current emission scenario, global mean temperature would rise between 0.9 and 3.5 degrees C by the year 2100. There are, however, many uncertainties that influence these predictions. Despite the significance of weather on plant diseases, comprehensive analysis of how climate change will influence plant diseases that impact primary production in agricultural systems is presently unavailable. Evaluation of the limited literature in this area suggests that the most likely impact of climate change will be felt in three areas: in losses from plant diseases, in the efficacy of disease management strategies and in the geographical distribution of plant diseases. Climate change could have positive, negative or no impact on individual plant diseases. More research is needed to obtain base-line information on different disease systems. Most plant disease models use different climatic variables and operate at a different spatial and temporal scale than do the global climate models. Improvements in methodology are necessary to realistically assess disease impacts at a global scale.

Potential impact of climate change on plant diseases of economic significance to Australia

Burning of fossil fuel, large scale clearing of forests and other human activities have changed global climate. Atmospheric concentration of radiatively active CO2, methane, nitrous oxide and chlorofluorocarbons has increased to cause global warming. In Australia temperature is projected to rise between 1 and 3°C by 2100. This review is the result of a recent workshop on the potential impact of climate change on plant diseases of economic significance to Australia. It gives an overview of projected changes in Australian climate and the current state of knowledge on the effect of climate change on plant diseases. Based on an assessment of important diseases of wheat and other cereals, sugarcane, deciduous fruits, grapevine, vegetables and forestry species, climate change in Australia may reduce, increase or have no effect on some diseases. Impacts will be felt in altered geographical distribution and crop loss due to changes in the physiology of host-pathogen interaction. Changes will occur in the type, amount and relative importance of pathogens and diseases. Host resistance may be overcome more rapidly due to accelerated pathogen evolution from increased fecundity at high CO2, and/or enhanced UV-B radiation. However, uncertainties about climate change predictions and the paucity of knowledge limit our ability to predict potential impacts on plant diseases. Both experimental and modelling approaches are available for impact assessment research. As the development and implementation of mitigation strategies take a long time, more research is urgently needed and we hope this review will stimulate interest.

Identity and pathogenicity of Fusarium spp. isolated from wheat fields in Queensland and northern New South Wales

To establish the identity of Fusarium species associated with head blight (FHB) and crown rot (CR) of wheat, samples were collected from wheat paddocks with different cropping history in southern Queensland and northern New South Wales during 2001. CR was more widespread but FHB was only evident in northern NSW and often occurred with CR in the same paddock. Twenty different Fusarium spp. were identified from monoconidial isolates originating from different plant parts by using morphology and species-specific PCR assays. Fusarium pseudograminearum constituted 48% of all isolates and was more frequently obtained from the crown, whereas Fusarium graminearum made up 28% of all isolates and came mostly from the head. All 17 Fusarium species tested caused FHB and all 10 tested caused CR in plant infection assays, with significant (P < 0.001) difference in aggressiveness among species and among isolates within species for both diseases. Overall, isolates from stubble and crown were more aggressive for CR, whereas isolates from the flag leaf node were more aggressive for FHB. Isolates that were highly aggressive in causing CR were those originating from paddocks with wheat following wheat, whereas those from fields with wheat following maize or sorghum were highly aggressive for FHB. Although 20% of isolates caused severe to highly severe FHB and CR, there was no significant (P < 0.32) correlation between aggressiveness for FHB and CR. Given the ability of F. graminearum to colonise crowns in the field and to cause severe CR in bioassays, it is unclear why this pathogen is not more widely distributed in Australia.

Comparative Pathogenomics Reveals Horizontally Acquired Novel Virulence Genes in Fungi Infecting Cereal Hosts

Comparative analyses of pathogen genomes provide new insights into how pathogens have evolved common and divergent virulence strategies to invade related plant species. Fusarium crown and root rots are important diseases of wheat and barley world-wide. In Australia, these diseases are primarily caused by the fungal pathogen Fusarium pseudograminearum. Comparative genomic analyses showed that the F. pseudograminearum genome encodes proteins that are present in other fungal pathogens of cereals but absent in non-cereal pathogens. In some cases, these cereal pathogen specific genes were also found in bacteria associated with plants. Phylogenetic analysis of selected F. pseudograminearum genes supported the hypothesis of horizontal gene transfer into diverse cereal pathogens. Two horizontally acquired genes with no previously known role in fungal pathogenesis were studied functionally via gene knockout methods and shown to significantly affect virulence of F. pseudograminearum on the cereal hosts wheat and barley. Our results indicate using comparative genomics to identify genes specific to pathogens of related hosts reveals novel virulence genes and illustrates the importance of horizontal gene transfer in the evolution of plant infecting fungal pathogens.

Potential impact of climate change on plant–pathogen interactions

How a rapidly changing climate may influence plant pathogens and the diseases they cause gained international prominence after Manning and Tiedemann (1995) first reviewed the impact of changing atmospheric CO2, O3 and UV-B on plant diseases. Two other publications considering changes in the biosphere and climate rapidly followed (Coakley 1995; Coakley and Scherm 1996). However, the effect of changing climate on plant diseaseswas assessed for NewZealand (Prestidge and Pottinger 1990) and the United Kingdom (Atkinson 1993) well before this and similar assessments have continued for other countries (Chakraborty et al. 1998), specific diseases/pathogens (Brasier and Scott 1994; Luo et al. 1995; Kaukoranta 1996; Bergot et al. 2004) and regions (Boland et al. 2004). Climate change effects on plant diseases have featured at many international meetings, including the Global Change and Terrestrial Ecology (GCTE) meeting at Reading in 1999 (http://mwnta.nmw.ac.uk/GCTEFocus3/ FoodandForest/99progr.htm). GCTE offers coordination among international groups for impact assessment (Scherm et al. 2000) on specific diseases such as potato late blight (Hijmans et al. 2000). Awareness among the plant pathology community was boosted by a session on this topic at the 7th International Congress of Plant Pathology (ICPP) in Edinburgh in 1998 (Chakraborty et al. 2000b). Since then there has been a session at the ICPP 2003 in Christchurch (Scherm and Coakley 2003) and one is planned for Turino in 2008. In Australia, a national workshop in 1997 addressed climate change impacts on economically significant plant diseases and a review was published in the Australasian Plant Pathology (Chakraborty et al. 1998). Although the topic has not yet sparked widespread interest among plant pathologists, new findings have continued to appear in plant pathology literature (Pangga et al. 2004) including novel approaches to impact modelling (Scherm 2004). Notable among recent empirical studies are diseases in natural plant communities using free air CO2 enrichment (FACE) (Percy et al. 2002), a field study on elevated temperature (Roy et al. 2004) and pathogen evolution (Chakraborty and Datta 2003). There have been important political developments too, none more significant than signing of the landmark Kyoto protocol and the recently announced ‘Asia-pacific partnership on clean development and climate’ between Australia, China, India, Japan, The Republic of Korea and the United States of America (http://www.pm.gov.au/news/media releases/media Release 1482.html). A plenary presentation by the author at the 15th Australasian Plant Pathology Society Conference, 26–29 September, 2005 in Geelong offered an opportunity to review current research and development in this area. This commentary reintroduces climate change to plant protection specialists, updates knowledge on its potential impacts on host-pathogen interactions to critically review progress and touches on future research needs in Australia to better manage diseases under a changing climate.

Plant adaptation to climate change—opportunities and priorities in breeding

Abstract. Climate change in Australia is expected to influence crop growing conditions through direct increases in elevated carbon dioxide (CO2) and average temperature, and through increases in the variability of climate, with potential to increase the occurrence of abiotic stresses such as heat, drought, waterlogging, and salinity. Associated effects of climate change and higher CO2 concentrations include impacts on the water-use efficiency of dryland and irrigated crop production, and potential effects on biosecurity, production, and quality of product via impacts on endemic and introduced pests and diseases, and tolerance to these challenges. Direct adaptation to these changes can occur through changes in crop, farm, and value-chain management and via economically driven, geographic shifts where different production systems operate. Within specific crops, a longer term adaptation is the breeding of new varieties that have an improved performance in ‘future’ growing conditions compared with existing varieties. In crops, breeding is an appropriate adaptation response where it complements management changes, or when the required management changes are too expensive or impractical. Breeding requires the assessment of genetic diversity for adaptation, and the selection and recombining of genetic resources into new varieties for production systems for projected future climate and atmospheric conditions. As in the past, an essential priority entering into a ‘climate-changed’ era will be breeding for resistance or tolerance to the effects of existing and new pests and diseases. Hence, research on the potential incidence and intensity of biotic stresses, and the opportunities for breeding solutions, is essential to prioritise investment, as the consequences could be catastrophic. The values of breeding activities to adapt to the five major abiotic effects of climate change (heat, drought, waterlogging, salinity, and elevated CO2) are more difficult to rank, and vary with species and production area, with impacts on both yield and quality of product. Although there is a high likelihood of future increases in atmospheric CO2 concentrations and temperatures across Australia, there is uncertainty about the direction and magnitude of rainfall change, particularly in the northern farming regions. Consequently, the clearest opportunities for ‘in-situ’ genetic gains for abiotic stresses are in developing better adaptation to higher temperatures (e.g. control of phenological stage durations, and tolerance to stress) and, for C3 species, in exploiting the (relatively small) fertilisation effects of elevated CO2. For most cultivated plant species, it remains to be demonstrated how much genetic variation exists for these traits and what value can be delivered via commercial varieties. Biotechnology-based breeding technologies (marker-assisted breeding and genetic modification) will be essential to accelerate genetic gain, but their application requires additional investment in the understanding, genetic characterisation, and phenotyping of complex adaptive traits for climate-change conditions.

Impacts of global change on diseases of agricultural crops and forest trees

The fourth assessment report of the Intergovernmental Panel on Climate Change projects rising levels of greenhouse gas and global temperature. The well-known dependence of plant diseases on weather has long been exploited for predicting epidemics and to time applications of control measures for tactical disease management. Fingerprints of inter-annual climatic variation on pathogens have recently been shown in literature linking pathogen abundance to atmospheric composition. Past reviews have dealt with impacts of changing atmospheric composition and climate on diseases, regional or country-wide assessments of climate change impacts and impacts on specific disease/pathogen or pathogen groups. All agree on paucity of knowledge prompting a need to generate new empirical data on host‐pathogen biology under a changing climate. Focused on experimental research, the purpose of this review is to summarize published and unpublished studies on plant pathogens and diseases in free-air CO2 enrichment (FACE) facilities and open top chambers and other current non-FACE research to offer a summary of future research needs and opportunities. Critical review of recent literature on the influence of elevated CO2 and O3 on agriculture and forestry species forms a major part of the treatise. Summaries of unpublished or ongoing experimental research on plant pathogens from FACE studies are included as a catalogue of work in this neglected area. The catalogue and knowledge gaps are intended as a resource for workers initiating research in this area as well as the general scientific community grappling with the design and scope of next generation of FACE facilities.

Pathogen population structure and epidemiology are keys to wheat crown rot and Fusarium head blight management

This paper summarises the key findings from recent research on the population genetics and epidemiology of Fusarium pathogens causing head blight and crown rot of wheat in Australia and how this information has enabled the screening and selection of wheat germplasm with improved resistance to Fusarium. By relating new findings to the current state of knowledge, the paper serves as a timely and critical review of the international literature. In Australia, both Fusarium pseudograminearum and F. graminearum can cause both crown rot and Fusarium head blight under artificial inoculation. However, the former species is more widespread and is predominantly associated with crown rot whereas F. graminearum is mainly associated with Fusarium head blight, with limited geographical distribution in and around the Liverpool Plains in northern New South Wales. Studies of population structure and genetics have revealed that both species are genotypically diverse with similar levels of genetic recombination despite Gibberella zeae, the teleomorph of F. graminearum, being homothallic and G. coronicola, the teleomorph of F. pseudograminearum, being heterothallic. A high-throughput and reliable crown rot bioassay has been developed and used to screen over 1500 wheat germplasms to select 17 lines with putative crown rot resistance. Key differences in pathogen biology and epidemiology between Australia and the USA have emerged from other recent collaborative studies, which show that macroconidia constitute the bulk of aerial Fusarium head blight inoculum in Australia, whereas ascospores are the dominant primary inoculum for Fusarium head blight worldwide. The limited spread of splash-dispersed macroconidia of F. graminearum probably explains the restricted geographical distribution of this species in Australia. Other research collaboration has compared the aggressiveness, mycotoxin production and genotypic polymorphisms of the pathogen population from Australia and the USA. These and other differences in pathogen adaptation emphasise that research outcomes from elsewhere must be tested for relevance before applying them to Australian farming systems.

Production and dispersal of Colletotrichum gloeosporioides spores on Stylosanthes scabra under elevated CO2.

This paper reports the effect of twice-ambient (700 ppm) atmospheric CO(2) concentration on infection, disease development, spore production and dispersal of the anthracnose pathogen Colletotrichum gloeosporioides in susceptible (Fitzroy) and partially resistant (Seca) cultivars of the tropical pasture legume Stylosanthes scabra under controlled environment and field conditions. Reduction in plant height due to anthracnose was partially compensated for by growth enhancement at elevated CO(2) in Fitzroy but not in Seca. Anthracnose severity was reduced under elevated CO(2) although the reduction was only significant in Fitzroy. Delayed and reduced germination, germtube growth and appressoria production were partly responsible for the reduced severity. Despite an extended incubation period, C. gloeosporioides developed sporulating lesions faster and produced more spores per day within the same latent period at high CO(2) and ambient CO(2). When Fitzroy seedlings grown at 700 ppm CO(2) were exposed to pathogen inoculum under field conditions, they consistently developed more severe anthracnose with more lesions than seedlings grown at ambient CO(2). The environmental variable, which correlated most strongly with the dispersal and infection of C. gloeosporioides spores in the field, was relative humidity in plant canopy. We have shown that an enlarged Stylosanthes canopy under elevated CO(2) can trap more spores, which can lead to more severe anthracnose under favorable weather. The implications of these findings for perennial Stylosanthes pastures are discussed.