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Sorghum Ergot Goes Global in Less Than Three Years

 

Prepared by G. Odvody (Texas A&M University), R. Bandyopadhyay (ICRISAT, Visiting Scientist, Texas A&M University), R. A. Frederiksen, T. Isakeit (Texas A&M University), D. Frederickson (Visiting Scientist, Texas A&M University), H. Kaufman (Texas A&M University), J. Dahlberg (USDA/ARS/TARS, Puerto Rico), R. Velasquez, H. Torres (INIFAP, Mexico & Texas A&M University)

doi:10.1094/APSFeature-1998-06

This article summarizes and updates a recent Plant Disease feature article (Plant Disease 82: 356-367, see link at left) where the reader can access more detailed discussion and relevant references. References here are restricted to those not cited in the feature article.

Global Spread and Distribution of Sorghum Ergot

In mid-1995, a widespread and economically important epidemic of Claviceps africana (sugary disease of sorghum, or ergot) was reported in commercial forage fields and F₁ hybrid production fields in Brazil. This was the first report of any sorghum ergot outside Asia and Africa. Prior to 1995, C. africana occurred primarily in Africa. Another Claviceps species, C. sorghi, is currently limited to the Indian subcontinent (figure 1). A third undescribed Claviceps spp. occurs only in Japan. Until classified as a distinct species in 1991, C. africana was considered synonymous with C. sorghi.

Sorghum ergot spread rapidly across South America and parts of Australia during 1996 and was observed in Mexico and the Carribean including Puerto Rico by February 1997 (1,7; figure 1). In Southern Tamaulipas and surrounding areas in adjacent states of Mexico sorghum ergot was a problem in hybrid seed production nurseries and commercial grain sorghum fields during the winter months where fields were exposed to cool temperatures that induced some sterility (7). Cool temperature sterility also appeared to increase incidence of ergot in johnsongrass.

By late March, 1997, it had been observed in the Lower Rio Grande Valley (LRGV) of Texas (3). The initial reports of ergot in northern Tamaulipas, Mexico and in the LRGV were on ratooned or "volunteer" sorghum plants from seed of the previous crop growing in abandoned fields. As the season progressed in the LRGV sorghum ergot was observed at low levels on the commercial grain sorghum crop and on some populations of johnsongrass. The incidence of ergot in the commercial grain sorghum crop in South Texas was minimal (generally one to several florets on less than 1% of the heads) and sometimes nondetectable. However, this incidence was higher than expected for grain sorghum hybrids because their self-fertility usually gives them a high level of postfertilization acquired resistance to the disease. Commercial hybrid seed production fields of sorghum in Tamaulipas and in the LRGV had some low levels of ergot primarily in late-season axillary tillers of the seed parent.

Following the progressive maturity of the sorghum crop across Texas and weather patterns that sporadically favored development, sorghum ergot continued its spread across the state and reached the hybrid seed production region of the Texas High Plains in August, 1997. This region has approximately 250,000 acres (>100,000 ha) of sorghum hybrid seed production fields that are at risk to ergot. Hybrid sorghum seed produced here represents about 90% of U.S. and 35% of the world production (Source: National Grain Sorghum Producers Association, Abernathy, Texas). Despite reports of high losses to ergot in hybrid seed production elsewhere (10 to 80 % in India, 12 to 25 % in Zimbabwe) ergot caused minor problems in Texas hybrid seed production fields in 1997. The primary impact of ergot was harvest and handling problems encountered in a few fields where seed parents had a high level of ergot in axillary tillers (figure 2; figure 3). These axillary tillers, also called stem tillers or suckers, were extremely vulnerable to development of ergot because they emerged late in crop development when no pollen was available to permit rapid fertilization. Ergot on late-season tillers of some females lines will likely be a sporadic and continuing problem until the disease is either controlled on these tillers or tillering itself is prevented or minimized.

By October, sorghum ergot had spread across the major sorghum producing regions of the Great Plains states (Kansas and Nebraska) and into some of the Southeast states such as Georgia and Mississippi (9) (figure 4). Sorghum ergot has also continued to spread across most sorghum growing regions of Mexico (7,8).

Biology of Sorghum Ergot

The rapid spread of C. africana and its unknown potential as an ongoing disease risk for production and consumption of grain sorghum has produced great interest in the pathogen. Some previously established biological characteristics about C. africana are being questioned because of a possible change in the pathogen that may be responsible for its rapid global distribution. However, we must also consider that what appears to be a changed pathogen may actually be the same pathogen that is simply responding to new, geographically diverse environments and hosts. Studies of genetic variability have been initiated by numerous scientists and an understanding of the basic biology of C. africana is an additional crucial component in this research. Furthermore, development of control methodologies and disease predictive models require additional knowledge about the differing potential for incidence of ergot and its survival across these vast new regions of occurrence.

Two key factors in the life cycle and epidemiology of  Claviceps africana are that 1) it is a specialized pathogen that attacks only nonfertilized ovaries and 2) airborne secondary conidia are the most important inoculum. Aerial conidia are the principal inoculum for repeating infection cycles that culminate in the rapid increase and spread of ergot within and between fields over vast areas.

A conidium deposited on the stigma of a flowering sorghum spikelet germinates to produce a germ tube that grows down the style and into the unfertilized ovary where it establishes the infection within 36 to 48 hr (figure 5). Within 5 to 10 days the sorghum ovary is converted into a whitish fungal mass called a sphacelium which pushes apart the glumes like an oversized seed (figure 6). A day later the sphacelium begins production of conidia (macroconidia) that are immersed in a nearly clear sugary liquid (figure 7; figure 8) which takes on an opaque, yellow-brown (figure 9) or orange to pink color (figure 10) because of the conidia. The conidia and liquid mixture is called honeydew. The syruplike honeydew is exuded onto the surface of the sphacelia and continues to drip down across the sorghum head (figure 11), and onto other plant parts and the soil surface. These conidia have limited capacity to spread because of their occurrence in a sticky liquid environment. When exposed to relative humidity above 90% the hygroscopic honeydew droplets acquire an increased water content (higher osmotic potential) at their outer surfaces which stimulates germination of the macroconidia at that location. These macroconidia germinate with the production of a conidiophore which penetrates the surface of the honeydew droplet and grows into the aerial environment where it produces a secondary conidium at its tip (figure 12). The honeydew is now much thinner in consistency and white in color at the surface. Because the secondary conidium is produced outside of the liquid environment it is now easily windblown to nearby or distant stigmas of susceptible sorghum florets. The amount of sporulation can be so massive that an entire sorghum head may develop a dusty white appearance (figure 13). Other areas like leaf and soil surfaces where dripping honeydew has fallen also take on a white appearance from the aerial conidia and conidiophores (figure 14; figure 15a; figure 15b).

Despite the massive production of aerial conidia there would be little or no infection unless the conidia were deposited on susceptible host tissue which is the stigma of a nonfertilized sorghum ovary. The fertilized ovary within a sorghum flower is resistant or immune to infection by C. africana. If a pollen grain and a conidium of C. africana are simultaneously deposited on the same stigma the pollen would normally complete fertilization within 2.5 to 12 hr and easily prevent infection by the slower-growing pathogen which requires 36 to 48 hr to complete infection at the base of the ovary. Therefore, anything which promotes rapid fertilization prevents or reduces incidence of ergot. Conversely, anything which either prevents or delays pollination and fertilization can favor infection by C. africana if inoculum of the pathogen is present. Male-sterile sorghums are highly susceptible to infection by ergot pathogens because they are dependent upon an outside source of pollen for fertilization. Self-fertile forage sorghums and sorghum-sudan hybrids have a variable vulnerability to infection by C. africana because they are often poor pollinators or have incomplete fertility and some are completely sterile. Most inbred lines and hybrids of grain sorghum are highly self-fertile and usually have a negligible or reduced-incidence of ergot under most environments. However, self-fertile sorghums may become highly vulnerable to ergot if they are exposed to temperatures below 12 C (54 F) in the 3 to 4 wk prior to bloom because these environments reduce pollen viability (4). Even lower temperatures may cause an immediate reduction in pollen viability and other environments such as wet and cloudy weather may also interfere with pollination/fertilization events.

Ergot is favored by mean temperatures of 19-21 C (66-70 F) and by high relative humidities (100%, optimal). The range of environments over which C. africana can cause infection are temperatures from 14-28 C (57-82 F) and relative humidities down to 67%. Incidence and severity of ergot at the limits of these environments can still be significant on highly susceptible sorghum hosts or in those cases where the effect of environment on the host is of greater importance than its effect on the pathogen. Experience in the U.S. in 1997 indicates that infection can occur readily at very high day temperatures up to 38 C (100 F) in the field if there is a nearby source of inoculum and nightly conditions are somewhat conducive for secondary conidiation. The primary effect of high temperatures may be their association with lower relative humidities that reduce secondary sporulation and limit the longevity of aerial conidia and the distance over which they can be effectively dispersed. Yield is directly reduced by ergot because individual florets infected within sorghum heads produce no grain. Sugary exudates from infected florets further contribute to a lowering of seed quality in seed that is produced because the sticky sugary mass encourages other fungal growth, interferes with harvest, and may necessitate other postharvest sanitation treatments of seed. Because nonfertilized florets of male-sterile sorghums are highly susceptible, the disease has tremendous impact on hybrid seed production in which cytoplasmic male-sterile lines are used as female parents.

Sclerotial Production and Survival of C. africana

Under continued dry conditions ergot sphacelia may slowly develop into solid dense sclerotia (usually slightly bigger than the size of seed).  Sclerotia may fail to develop if conditions remain wet and humid because saprophytic fungi colonize remaining honeydew and ergot tissues; this colonization produces whole heads or individual sphacelia that may be completely black in appearance (figure 16). Sclerotia are long term survival structures of C. africana that fall to the soil or may be harvested with the seed. These structures may germinate in soil to produce a sexual structure (figure 17) and aerially-disseminated sexual spores called ascospores. Functional sclerotia in ergot-contaminated seed have been suggested as a possible means of ergot introduction into the Americas and Australia. Other theories of introduction include long distance dispersal of conidia on wind currents or in honeydew either coating sorghum seed or sticking to sorghum workers’ shoes or clothing. The sclerotia (and honeydew), especially in hybrid seed, have also been suggested as a possible vehicle for survival and spread within the Americas but their role is unknown. The primary reason for uncertainty is that very few sclerotia of C. africana have ever been germinated so they do not appear to be a primary or consistent method by which the pathogen is spread and their role in survival is unknown. However, sclerotia (or dried sphacelia) may contain viable macroconidia of C. africana inside internal cavities. Commercial companies in Brazil and the U.S. can remove sclerotia or sclerotia-like bodies of ergot (figure 18) from contaminated seed to almost nondetectable levels using their standard seed-conditioning equipment. Healthy seed may be encrusted with dried honeydew containing viable macroconidia of C. africana (figure 19) but they are easily killed by seed treatment with standard contact fungicides
(http://www.ars-grin.gov/ars/SoAtlantic/Mayaguez/seedtmt.html) (2).

Host range and genetic variability of C. africana

Sorghum spp., including feral or wild sorghums like johnsongrass (figure 20), appear to be the primary hosts for C. africana. Some other grasses have been reported as hosts of C. africana in Africa but there is uncertainty about their status as true hosts and none have been confirmed as hosts in the Americas. There has been much speculation that the strains of C. africana now spreading across the globe may be substantially different from some of those existing in Africa. Scientists at various U.S. and international locations are using traditional and biotechnological approaches to determine the genetic relatedness between strains from different geographical regions. Identification of genetic differences would necessitate a re-evaluation of C. africana and the major differences between strains, especially as they may relate to epidemiology, survival, toxicity, and virulence.

Survival of Claviceps africana in Mexico and the U.S.

Survival of C. africana in the Americas is being evaluated across diverse environments including the variable winter environments of the Northern Plains states of the U.S. The mechanism of survival and the source of initial inoculum in the current growing season will be of great interest because true sclerotia have been difficult to identify in the Americas. Johnsongrass may be one of the primary overwintering reservoirs for C. africana but there is uncertainty about the ability of the pathogen to survive the low temperatures and freeze-thaw cycles of the winters in the Plains states.

Claviceps africana was continually present as far North as Corpus Christi, Texas on ratoon and "volunteer" sorghum escaping frost during the mild winter of 1997-98. Similarly, in the humid region of Southern Tamaulipas, Mexico, ergot incidence was high in seed production fields that flowered during December, 1997 to January, 1998. Incidence of ergot was often high because cool temperatures induced sterility in johnsongrass and other self-fertile sorghums. A similar persistence of ergot is assured in many areas of Mexico where sorghum is produced during the winter months and there is usually no frost to kill johnsongrass and feral sorghums along roadsides and in abandoned fields. However, during the 1998 spring season, not a single sorghum flower has been reported with ergot in the important sorghum-producing region of Northern Tamaulipas, Mexico, where the growing season has been dry and hot. In the current U.S. crop that is past bloom (LRGV and South Texas) sorghum ergot has been detectable at low levels only in sorghums directly adjacent to areas of winter survival and virtually nondetectable in commercial sorghum fields. The extremely dry environments in Mexico and South Texas have severely limited ergot development and spread.

Sorghum Hosts Most Vulnerable to Ergot

Claviceps africana (and other Claviceps spp.) attack only nonfertilized ovaries so sorghums most susceptible to ergot are male-sterile sorghums including those used as seed parents in hybrid seed production. Ergot appears to be a minor threat to commercial grain sorghum production except where environmental factors interfere with self-fertility that normally prevents sorghum ergot. Preliminary evidence suggests that some commercial hybrids are more prone to loss in self-fertility, and therefore are more susceptible, than others under similar environmental conditions. Although the potential for ergot in commercial grain sorghum fields is minimal the dependence on hybrid seed for planting those fields puts the producer and the entire sorghum industry at some risk. The higher potential for ergot in hybrid seed production fields may affect the quality, cost, and availability of some hybrid sorghum seed. Until host plant resistance is present in commercially useful male-sterile sorghums it will be necessary to utilize other integrated control methodologies including pollen management, chemicals, and other alternate control strategies.

Host Plant Resistance

In self-fertile sorghums, much of the identified host plant resistance to ergot may be an acquired type of resistance related to maintenance of high self fertility under environments in regions of adaptation and testing. This resistance is often lacking when these sorghums are evaluated at other geographic locations. Interaction between environment and various fertility factors of lines and hybrids are being investigated globally including cool temperature pollen sterility and flowering synchrony.

Resistance to ergot based on self-fertility factors would be non-functional in male-steriles. All male-sterile sorghums appear to be susceptible to C. africana but relative differences in susceptibility noted between some lines may be due to other factors such as length of female receptivity. Unique characteristics of fertilization for specific male:female inbred combinations are among several other factors being investigated to identify characteristics that may contribute to either susceptibility or resistance.

Biotechnological approaches to incorporate fungitoxic principles in sorghum pistils may provide new avenues to accomplish ergot resistance in agronomically desirable sorghums.

Integrated Control of Sorghum Ergot

Any factor ensuring maximum pollination/fertilization of the male-sterile parent directly reduces the risk of sorghum ergot. Pollen management techniques such as reduction of female:male row ratios, multiple planting dates of male pollinators, and field capping cropping practices are some of the current methods being employed by the industry (figure 21). Commercial seed producers know that variable flowering and other characteristics of individual seed parent lines will become even more important now that ergot is an additional threat to seed set and the production of quality hybrid seed.

Triazole fungicides have been effectively used to control sorghum ergot in hybrid seed production fields in the Americas and Australia since their initial field use in Brazil. Systemic translocation within the host tissues is apparently necessary to stop infection by C. africana because contact fungicides are ineffective in field applications. The most effective application methods have combined ground application with a head-directed spray of the fungicides (figure 22). The vast acreage and wet soils of irrigated U.S. hybrid seed production fields indicate that aerial application may be the only method that will allow timely application of triazole fungicides to control ergot (6).

Following crisis exemptions and section 18 approval to apply Tilt (propiconazole) for ergot control in 1997, a similar section 18 was granted in 1998 primarily for use in hybrid seed production fields (http://www.agr.state.tx.us/pesticide/tilt98.htm). The label allows Tilt to be applied at 125 g a.i./ha (4 oz/ac of Tilt 3.6E [41.8% by wt], 0.113 lb a.i./ac) in each of three applications for a total of 375 g a.i./ha (12 oz product/ac)(6). A generally low and variable incidence of ergot in Texas hybrid seed production fields in 1997 has produced some industry uncertainty concerning efficacy of aerial applications especially at common application volumes of only 47 liters/ha (5 gal/ac).

Quarantine and Movement of Seed Between Ergot Areas

There is no apparent need to restrict or quarantine seed movement between regions where ergot has been previously observed. Ergot probably can be introduced on nontreated, contaminated seed but fungicide seed treatments with captan or thiram on hybrid seed should prevent dissemination (http://www.ars-grin.gov/ars/SoAtlantic/Mayaguez/seedtmt.html) (2). In those rare instances when fungicide-treated seed still produces some aerial inoculum of C. africana, a susceptible host in the bloom stage must simultaneously be present before infection can occur. Although this method could potentially spread the pathogen to new regions reintroduction will likely be insignificant because other local inoculum sources will probably be more consistently available. If local inoculum sources are low due to reduced survival of C. africana in northern sorghum growing regions, aerial spread from southern regions may still be a more important source of inoculum than reintroduction through seed.

Toxicity of Ergot Contaminated Sorghum

Previous animal feeding studies demonstrated minimal toxicity of both the sclerotia of C. africana and dihydroergosine, the predominant, unique alkaloid within sclerotia. However, recent information from Australia indicated toxicity to poultry and swine that were fed grain contaminated with up to 5% sclerotia of C. africana (http://www.ars-grin.gov/ars/SoAtlantic/Mayaguez/feed.html). Varying the amounts of ergot sclerotia produced feed which had alkaloid contents of 0.002-0.005% of which approximately 90% was dihydroergosine. The high levels of ergot were restricted to a few very late-planted commercial grain sorghum fields in Australia that bloomed during cool temperature environments. Dry, cool environments after infection apparently allowed production of true sclerotia. Similar poultry and other animal feeding trials are being conducted or planned in the U.S. using tailings (screenings or discarded material) of conditioned grain from a few hybrid seed production fields heavily infected by ergot (figure 18). Dihydroergosine has been easily detected in sphacelia/sclerotia from these materials (Richard Shelby, Auburn University and James Porter, USDA-ARS, Athens, GA, Personal communication, http://www.ars-grin.gov/ars/SoAtlantic/Mayaguez/akaloid.html).

Global Research and Collaboration

As C. africana became a global threat over the previous three years there was an intensification of research efforts that culminated in the Global Conference on Ergot of Sorghum held June 1 to 8, 1997 in Sete Lagoas, Brazil. In addition to information exchange, the conference developed recommendations in the following research and related areas: 1) epidemiology (natural and human-aided dispersal) and disease predictive models; 2) alternate hosts for C. africana and other sorghum ergots; 3) survival mechanisms and structures and sources of initial and secondary inoculum; 4) identification of genetic sources of resistance and mechanisms of resistance; 5) integrated control including fungicides, pollen management, and other methods; 6) genetic characterization of variability in C. africana; 7) toxicity to animals of grain and stover from ergot-affected fields; and 8) utilization of molecular approaches to differentiate Claviceps species, characterize populations within species, and develop sorghum host plant resistance. A U.S. Conference on Sorghum Ergot held in Amarillo, TX on June 11, 1997 further delineated our current knowledge and projected areas for ergot research in the U.S. (5). Another conference, Status of Sorghum Ergot in North America, is scheduled for June 24-26, 1998 at the Omni Hotel in Corpus Christi, Texas. Details on the conference can be obtained at
http://www.ars-grin.gov/ars/SoAtlantic/Mayaguez/program.html.

Many informal linkages were established during the global spread of ergot to provide for the rapid exchange of ergot information via email, websites, and other methods of communication. Electronic communication was invaluable to global efforts in tracking the pathogen and in the timely exchange of scientific information for immediate application by scientists everywhere. This communication has fostered a cooperative attitude and approach that involves nearly every aspect of the sorghum industry including research scientists and others representing public and private institutions from various countries, national and state regulatory agencies, commodity or trade organizations and scientific societies like APS. This broad-based approach encourages dissemination of research information and is necessary because many objectives are regional or global in scope. An NCR project, NCR-501, was established in 1997 to develop collaborative sorghum research efforts among states most affected by sorghum ergot and among scientists who will be conducting this research.

The primary research perspective is to provide control methods for those areas of the sorghum industry most immediately threatened by ergot. Those efforts involve development of integrated controls for C. africana in hybrid seed production fields with emphasis on chemical and agronomic controls including pollen management. These controls will help reduce the immediate impact of sorghum ergot on the hybrid seed production industry until adequate host plant resistance and other appropriate control methodologies are developed and more definitive biological information about C. africana is available.

Acknowledgments

Others making contributions to the information presented in this article and colleagues collaborating on sorghum ergot from other states and institutions: J. Stack, S. Jensen (University of Nebraska), D. Jardine, L. Claflin, K. Kofoid, M. Tunistra, J. Leslie (Kansas State University), B. Rooney , C. Rush, J. Krausz (Texas A&M University), M. Ryley (Queensland Department of Primary Industries, Australia), N. McLaren (Grain Crops Research Institute, South Africa), P. Tooley (USDA-Frederick, MD), J. Porter (USDA-ARS, Athens, GA), R. Shelby (Auburn University), and T. Lust (National Grain Sorghum Producers Association, Abernathy, TX).

References

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