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2007 Plant Management Network.
Accepted for publication 10 July 2007. Published 8 November 2007.


Brown Stripe Downy Mildew (Sclerophthora rayssiae var. zeae) of Maize


Melodie L. Putnam, Botany and Plant Pathology, Oregon State University, Corvallis 97331


Corresponding author: Melodie L. Putnam. putnamm@science.oregonstate.edu


Putnam, M. L. 2007. Brown stripe downy mildew (Sclerophthora rayssiae var. zeae) of maize. Online. Plant Health Progress doi:10.1094/PHP-2007-1108-01-DG.


Introduction

The Congressional Public Health Security and Bioterrorism Preparedness and Response Act of 2002 charged the US Secretary of Agriculture to "by regulation establish and maintain a list of each biological agent and each toxin that the Secretary determines has the potential to pose a severe threat to animal or plant health, or to animal or plant products." From this Act was promulgated a list of Select Agents deemed particular threats to plant health. One of these is the pathogen Sclerophthora rayssiae var. zeae, cause of brown stripe downy mildew, which also appears on the USDA Animal and Plant Health Inspection Service (APHIS) list of regulated plant pests (5).

Maize (Zea mays) is the most widely produced grain in the United States. Nearly 32 million hectares of land were planted to maize in 2005 (1). In India, where the brown stripe downy mildew pathogen was first discovered, yield losses from brown stripe downy mildew range from 20 to 90% (3). Greatest losses have been experienced in areas of high rainfall where susceptible cultivars have been grown (8). Even if only 20% of the crop in the US were seriously affected, this could translate into a $4 billion loss (calculated at 2005 prices). Because of this potential impact, rapid detection and diagnosis of brown stripe downy mildew is essential. The National Plant Diagnostic Network (NPDN) is a consortium of federal, state, and university laboratories established to aid in rapid detection and reporting of pest and pathogen outbreaks (12). The NPDN has established protocols for recognition of Select Agents for participating laboratories. Due to the potential impact of an introduction of brown stripe downy mildew, this information is being widely disseminated so that suspect samples can be quickly and correctly identified.


Host: Maize (Zea mays L.)


Disease: Brown stripe downy mildew


Pathogen: Sclerophthora rayssiae var. zeae Payak & Renfro 1967


Taxonomy

The fungus is described by Payak and Renfro (7). The current taxonomic status is listed online in the CABI Index Fungorum (4).


Symptoms and Signs

Sclerophthora rayssiae var. zeae causes leaf lesions only (7). In early stages of infection leaves will show narrow chlorotic or yellowish stripes, 3 to 7 mm wide (Fig. 1); in some maize genotypes, these stripes will be reddish to purple. The lesions have well defined margins and extend parallel with and are delimited by the leaf veins. Advanced striping and blotching occurs with confluence of adjacent lesions. The disease may first be noticed on the lower leaves, which will show the greatest degree of striping; as a result they appear pale-brown and burnt, and severely affected leaves may be shed prematurely. S. rayssiae var. zeae infection has been associated with smaller seed size (6). Early plant death can result when severe disease occurs prior to flowering. Unlike other downy mildews of maize, brown stripe downy mildew does not result in malformation of vegetative or floral tissues. The pathogen apparently does not systemically infect the plant (8).


 

Fig. 1. Symptoms of brown stripe downy mildew. Image courtesy C. De Leon. Reproduced, with permission, from Compendium of Corn Diseases, 3rd Ed., 1999, American Phytopathological Society, St. Paul, MN.

 

Under conditions of high moisture, sporangial growth appears as a grayish-white woolly growth on both the upper and lower surfaces of lesions. Sporangia disappear as the lesions become necrotic. Oospores occur only in necrotic tissues, in the mesophyll or beneath the stomata, but not in vascular tissue.


Host Range

The primary host is Zea mays L. (maize). The organism can also infect Digitaria sanguinalis (L.) Scop. (large, or hairy crabgrass), which may act as a source of inoculum for early sown maize under favorable environmental conditions (2). Digitaria bicornus (Lam.) Roem. & Schult. (southern crabgrass) in Thailand was found infected with S. rayssiae var. zeae, but this strain of the pathogen was not capable of infecting maize (3). Susceptibility of other grasses via natural infection has not been reported. Inoculation experiments using several unspecified species of millets, cereals, and grasses were unsuccessful (11).


Geographic Distribution

This disease was first observed in several maize growing areas of India in 1962 (7), and since then it has spread throughout India, and has been reported from Myanmar, Nepal, Pakistan, and Thailand (3).

Brown stripe downy mildew incidence is greatest in regions of high rainfall. In India the worst epidemics have been in areas that receive 100 to 200 cm of rainfall annually. Disease also occurred in regions where average annual rainfall was roughly 50 to 70 cm, but incidence was light. Moderate disease incidence has been recorded in India where average annual rainfall was 60 to 100 cm (7).


Transmission

Primary inoculum comes from oospores overseasoning in soil or plant debris or from mycelium in infected seed.

Maize seed may be contaminated in two ways. The seed surface may carry plant debris containing viable oospores (6), and the seed may carry oospores or mycelium within the embryo (6,9). Disease can become established on seedlings grown from infected seed (9), although seed transmission was found to occur at less than 1% (6), and it is likely that infected leaf debris is more important than seed in initiating new infections (8). Oospores in air-dried leaf tissue can remain viable for 3 to 5 years (8,11), although infected seed dried to 14% moisture or less and stored for 4 or more weeks will not be capable of transmitting the disease (13).

Oospores generally undergo indirect germination, producing sporangiophores that bear sporangia which may contain four to eight zoospores. Less frequently, the sporangium may germinate directly and produce a germ tube capable of penetrating maize leaves. Rapid spread of the pathogen in the field occurs with the production of sporangia (secondary inoculum), which are dispersed in wind and water splash, or from physical contact with an infected plant. Sporangia have been trapped 1.65 m from an infected field, but the greatest numbers of sporangia were found to move less than 1 m, suggesting long distance transport via wind is unlikely (10).

Moisture is essential for infection by S. rayssiae var. zeae (9,11). Sporangia production, germination, and infection require a film of water. Twelve hours of leaf wetness were required for infection via zoospores, with longer periods producing greater numbers of infected plants. Most sporangia are liberated at maturity during the day (11). Sporangial release occurs in the afternoon of sunny days when high moisture is present, rather than on cloudy or rainy days (10). Generation time of secondary inoculum (sporangia) from primary inoculum (oospores) can be rapid. Under ideal conditions, sporangial production can occur as soon as 10 days post-inoculation. Sporangia are produced over a wide range of temperatures (18 to 30C), but are most abundantly produced at 22 to 25C. Infected leaves placed in a moist environment at 22 to 25C can produce sporangia in as little as 3 h, with a second generation of sporangia arising 9 h later (11). Young plants are most susceptible to inoculation, with susceptibility decreasing as the plants age (11).

Warm soil (28 to 32.5C) is required for disease development when seeds are inoculated with infected plant debris (11). There is no information on the ability of the pathogen to withstand winter temperatures in northern climates.


Economic Importance

S. rayssiae var. zeae causes severe infection on susceptible maize genotypes in areas of high rainfall, where the disease is common and can occur at 20 to 70% incidence. In some locations disease incidence can be as high 100% (8). Losses are greatest in regions with abundant summer moisture and warm soils.

According to CABI (3), losses due to the disease vary depending on when and how severely the tissue is affected. If three-quarters or more of the foliage is affected prior to flowering, then the loss may be total; ear formation is either totally suppressed or markedly attenuated. Grain yield reductions vary from 20 to 90%. Losses in the higher range occur only with highly susceptible cultivars in conditions conducive for disease development.

Maize genotypes vary in their reaction to S. rayssiae var. zeae (7) Among 2113 Indian maize inbred lines and other germplasm scored in the field, 58 were highly resistant, 667 resistant, 772 moderately resistant, 478 susceptible, and 138 highly susceptible (9).


Pathogen Isolation

Sclerophthora rayssiae var. zeae is an obligate parasite and does not grow in artificial culture.


Pathogen Identification

Brown stripe downy mildew of maize is a Select Agent as defined by the USDA APHIS. This means possession of the pathogen is strictly regulated and the person possessing the pathogen is subject to prosecution if the diseased material is not handled in accordance with federal regulations. If this disease is suspected, notification of state and federal regulatory officials is required. Samples should be sent to the local state Department of Agriculture, federal Plant Protection and Quarantine office, or the nearest participating National Plant Diagnostic Network laboratory, which has standard operating procedures by which brown stripe downy mildew may be diagnosed and the correct officials notified. State regulatory officials are listed at the National Plant Board's membership page; NPDN labs for each state can be found at the NPDN's website. Samples must be double bagged in self-sealing plastic bags and mailed in a crush-proof container with all seams taped to prevent escape of diseased material. Contact the nearest regulatory official or NPDN laboratory for additional information on the procedure for submitting samples.


Morphological identification of S. rayssiae var. zeae:


Sporangiophores are short, determinate, and produced from hyphae in the substomatal cavities.


Sporangia are formed sympodially in groups of two to six, arising in basipetal succession. Sporangia are hyaline; ovate, obclavate, elliptic or cylindrical; smooth-walled; and are papillate, possessing a projecting truncate, rounded or tapering poroid apex. The sporangia are caducous, with a persistent, straight or cuneate peduncle. Sporangia range in size from 18.5-26.0 m 29.0-66.5 m; there may be lens shaped pores through which zoospores or cytoplasm may escape. Four to eight zoospores are formed in the sporangia and may encyst within or outside of it.


Zoospores are hyaline, spherical, and vary from 7.5 to 11.0 m in diameter.


Oogonia are hyaline to light and 33.0 to 44.5 m in diameter. Thin-walled, they may have one or two paragynous antheridia.


Oospores are pleurotic, spherical or subspherical; and are hyaline, with one prominent oil globule. Cell walls are smooth, glistening, and uniformly about 4 m thick, confluent with the oogonial wall. They range from 29.5 to 37.0 m in size.


Sporangia production may be stimulated by placing chlorotic symptomatic tissue into a moist chamber and incubating at 22 to 25C. Necrotic tissue will not produce sporangia. Sporangia should be produced within 3 to 9 h.

Oogonia and oospores are produced in necrotic tissue and may be visualized by clearing the leaf tissues in 2% sodium or potassium hydroxide solution at 45 to 50C, washing in several changes of distilled water, then staining with 0.1 % cotton blue (= methyl blue) in 50% glycerin for up to 20 min at 45 to 50C. Exact times for initial clearing and staining of tissues will vary depending on maturity and thickness of the tissues. Leaves should take less than 1 h to clear.

Chlorotic striping of maize leaves may be due to both abiotic and biotic factors. Maize in the US is susceptible to other downy mildew diseases, including sorghum downy mildew, caused by Peronosclerospora sorghi, and crazy top, caused by Sclerophthora macrospora (13). Brown stripe downy mildew is not a systemic disease, and the pathogen will only be present in infected leaves. Other characters distinguishing the brown stripe downy mildew pathogen from other downy mildew pathogens common in the US are in Table 1.

Sclerophthora macrospora (cause of crazy top) causes leaf or floral malformation or distortion (Fig. 2), which is absent with brown stripe downy mildew. Sporangia and oospores are larger than those of S. rayssiae var. zeae; oospores develop mainly in vascular bundles or in their parenchymatous sheath cells, whereas oospores of S. rayssiae var. zeae do not occur in vascular bundles. Sporangia of the crazy top pathogen form rarely on plant material in the field. In contrast, the brown stripe downy mildew pathogen forms sporangia readily in pre-necrotic leaf tissues in the field under conditions of high humidity.

Peronosclerospora sorghi systemically infects plants, causing stunting and linear to irregular whitish yellow-stripes on leaves. Affected leaves always have chlorosis of the base of the blade (Fig. 3) with a sharply defined transverse margin between diseased and healthy tissue. No purpling or reddish color develops in affected tissues.


Table 1. Comparison of brown stripe downy mildew with two downy mildews that occur on Zea mays in the United States.

Comparison Crazy top
(Sclerophthora macrospora)
Sorghum downy mildew
(Peronosclerospora sorghi)
Brown stripe downy mildew
(Sclerophthora rayssiae var. zeae)
Oospore* diameter & location in plant 45-75 μm
Mostly in vascular bundles or in their parenchymatous sheath cells
25-43 μm (36 μm avg)
In mesophyll
30-37 μm
Only in mesophyll or substomatal cavities
Secondary inoculum* Sporangia lemon-shaped, operculate;
30-65 60-100 μm
Conidia obovate, non-papillate, non-poroid;
15-29 15-23 μm
Sporangia ovate, obclavate, elliptic or cylindrical; papillate, with a projecting truncate, rounded or tapering poroid apex;
18.5-26 29.0-66.5 m
Location of pathogen in plant Systemic Systemic Leaf blades and sheaths only

 * Size will vary depending on environmental conditions at time of formation.


     
 

Fig. 2. Infection of corn by Sclerophthora macrospora causes a characteristic malformation of floral structures. Here the ear shows phyllody. Photo courtesy of Gary Munkvold, Iowa State University.

 

Fig. 3. Symptoms of corn infected with Peronosclerospora sorghi, showing the characteristic white striping of leaves, which always includes the base. Photo courtesy of L. E. Claflin. Reproduced from Compendium of Corn Diseases, 3rd ed., 1999, American Phytopathological Society, St. Paul, MN.

 

Pathogen Storage

While examination and testing is being conducted, plant material suspected of infection by Sclerophthora rayssiae var. zeae (hereafter called suspect plant material) must be stored double-bagged in access-controlled cabinets or refrigerators.

Keeping the suspect plant material for extended periods of time is not recommended. If suspect plant material has been confirmed with brown stripe downy mildew, all tissues in possession must be destroyed using a biologically monitored autoclave. The autoclave must be set at a minimum of 103.4 kPa, 121C for 20 min. Supplies and materials contaminated during examination of the suspect plant material must also be suitably disinfected.


Acknowledgment

The author is indebted to Karen Rane and Paul Reeser for critically reviewing the manuscript.


Literature Cited

1. Anonymous. 2005. United States Department of Agriculture, National Agricultural Statistics Service (USDA-NASS). 2005. Agricultural statistics. Online. USDA-NASS, Washington, DC.

2. Bains, S. S., Jhooty, J. S., Sokhi, S. S., and Rewal, H. S. 1978. Role of Digitaria sanguinalis in outbreaks of brown stripe downy mildew of maize. Plant Dis. Rep. 62:143.

3. CAB International. 2006. Crop protection compendium. Online. CAB International, Wallingford, UK.

4. CAB International. 2004. Index Fungorum. Online. CAB International, Wallingford, UK.

5. Cline, E. T., and Farr, D. F. 2006. Synopsis of fungi listed as regulated plant pests by the USDA Animal and Plant Health Inspection Service: Notes on nomenclature, disease, plant hosts, and geographic distribution. Plant Health Progress doi:10.1094/PHP-2006-0505-01-DG.

6. Lal, S., and Prasad, T. 1989. Detection and management of seed-borne nature of downy mildew diseases of Maize. Seeds Farms 15:35-40.

7. Payak, M. M., and Renfro, B. L. 1967. A new downy mildew disease of maize. Phytopathology 57:394-397

8. Singh, J. P. 1971. Infectivity and survival of oospores of Sclerophthora rayssiae var. zeae. Indian J. Exp. Biol. 9:530-532.

9. Singh, R. S., Joshi, M. M., and Chaube, H. S. 1967. Further evidence of the seedborne nature of maize downy mildews and their possible control with chemicals. Plant Dis. Rep. 52:446-449.

10. Singh, J. P., and Renfro, B. L. 1971. Studies on spore dispersal in Sclerophthora rayssiae var. zeae. Indian Phytopath. 24:457-461

11. Singh, J. P., Renfro, B. L., and Payak, M. M. 1970. Studies on the epidemiology and control of brown stripe downy mildew of maize (Sclerophthora rayssiae var. zeae). Indian Phytopath. 23:194-208.

12. Stack, J., Cardwell, K., Hammerschmidt, R., Byrne, J., Loria, R., Snover-Clift, K., Baldwin, W., Wisler, G., Beck, H., Bostock, R., Thomas, C., and Luke, E. 2006. The National Plant Diagnostic Network. Plant Dis. 90:128-136. DOI:10.1094/PD-90-0128.

13. White, D. G., ed. 1999. Compendium of Maize Diseases, 3rd Ed. American Phytopathological Society, St. Paul, MN.