Most infections of M. fijiensis and M. musicola begin with spores being deposited on the susceptible cigar leaf of the banana plant. Spores will germinate within 2-3 hours of being deposited on the leaf surface if there is a water film present or if the humidity is very high. The optimal temperature for germination of M. fijiensis spores is 27ºC. For M. musicola the optimal temperature for germination of conidia is between 25-29ºC and for ascospores it is between 25-26ºC. The germ tube then grows epiphytically for several days (2-3 days for M. fijiensis and 4-6 days for M. musicola) before penetrating the leaf via stomata in a hydrotropic response through the formation of appressoria or stomatopodia over the stomata (Meredith 1970; Stover 1980).
Once inside the leaf, the infection hypha forms a large substomatal vesicle. Fine hyphae then grow through the mesophyll layers into an air chamber and then into the palisade tissue. From here the hyphae grow out into other air chambers eventually emerging through stomata in the streak that has developed. Again, epiphytic growth occurs before the re-entry of the hypha into the leaf through another stomate.
Conidia are observable from stage 2 of black Sigatoka whereas they are generally only visible from stage 4 of yellow Sigatoka. Perithecia form during stages 5 and 6 of black Sigatoka and during stage 5 of yellow Sigatoka. Overall the disease cycle is much faster for M. fijiensis than for M. musicola due to shorter time required to complete the life cycle. Generally, it has been observed, the optimal conditions for M. fijiensis are those where there is, on average, higher temperatures and higher relative humidity. See Table 2 for the disease development and associated structures found during the disease cycle for each of these pathogens.
Comprehensive cytological studies of the interactions between M. fijiensis and three banana genotypes have been undertaken (Beveraggi et al. 1995) (Sallé et al. 1989). From these studies it was found that there is a relatively long period of biotrophy before any incompatible reactions are observed in susceptible cultivars. The pathogen colonises the leaf tissue, growing intercellularly without the production of haustoria, for almost a month. During this period, little evidence of the presence of the pathogen can be seen externally. Cytological changes are visible in the parenchyma cells after about 28 days although the cells still appear healthy. There is contact between the hyphae and the cells but no localised reaction. Externally, stage 2 or the initial streak stage symptoms are visible.
After 41 days, stage 5 or second spot stage symptoms are visible externally. In the tissue sections taken from the susceptible cultivar 'Grande Naine' at this time during the studies, three distinctive zones were seen. Zone I which corresponded to the cells within the necrotic spot contained plasmolysed cells. Zone II corresponded to the yellow halo and this region contained cells with large intracellular globules. At the boundary of Zones II & III an intercellular substance, later identified as polyphenol, was noted. This substance formed intercellular bridges and host cells in contact with it showed degeneration of the cell wall.
Beyond this boundary the remaining host cells in Zone III appeared to be healthy. Hyphae were observed throughout the intercellular spaces in all of the zones (Sallé et al. 1989). Importantly, haustoria were never observed during the invasion of any host by M. fijiensis. The progression of the disease was similar in the partially resistant cultivar, 'Fougamou', except that the growth rate of hyphae in the susceptible cultivar was much higher than in the partially resistant cultivar (Beveraggi et al. 1995; Sallé et al. 1989). In the highly resistant cultivar, 'Yangambi Km5', a compatible reaction was not observed. There was no biotrophic
period; rather fungal growth was blocked at the site of penetration. Stomatal guard cells became necrotic and there was a deposition of polyphenolic substances around the outside of the cell walls of the host and the pathogen. This is consistent with a hypersensitive response (Beveraggi et al. 1995; Sallé et al. 1989).
The Causal Agents
Black Sigatoka is caused by the heterothallic ascomycetous fungi Mycosphaerella fijiensis Morelet (anamorph Paracercospora fijiensis). Yellow Sigatoka is caused by another, Mycosphaerella musicola Leach ex Mulder (anamorph Pseudocercospora musae). Jones (2000) has a comprehensive chapter describing fungal leaf diseases of banana plants.
Disease Development and Epidemiology
The disease cycle for both M. fijiensis and M. musicola is similar with only minor differences as outlined previously. As M. fijiensis produces considerably less conidia and for a shorter period of time than M. musicola, ascospores are the main dispersal agent for this pathogen (Stover 1980). Both conidia and ascospores are important for dispersal of M. musicola(Stover 1971) however for both pathogens ascospores are involved in the movement of the pathogen over longer distances rather than conidia. A distinctive line spotting pattern of infection is produced when the source of inoculum is conidia dislodged by rain splashes. These run down the inside of the cigar leaf cylinder contacting the lower point of the cylinder resulting in a line of infection. The deposition of ascospores by wind currents is generally on the terminal end of these leaves resulting in a distinctive leaf tip infection (Meredith 1970; Stover 1972).
The disease cycle is much faster for black Sigatoka than it is for yellow Sigatoka, as seen by the earlier appearance of spots. Inoculation studies conducted in Honduras demonstrated that spotting associated with M. fijiensis infections appeared 8-10 days faster than that associated with M. musicola infections. Ascospore maturation time is also shorter at 2 weeks for M.fijiensis compared with 4 weeks for M. musicola (Stover 1980). A diagrammatic representation of the disease cycle for M. musicola is presented in Figure 1.
Figure 1: Life cycle of Mycosphaerella musicola, the fungal pathogen causing yellow Sigatoka (Reproduced with permission, Department of Primary Industries & Fisheries,Queensland).
Survival of the Inoculum
Production of perithecia and the subsequent discharge of ascospores continues for several months. Even in severely necrotic tissue, ascospore ejection can continue for more than two months, this is the case also where the leaf has been removed and placed on the ground (Carlier et al. 2000a). Ascospore release remains high for three weeks after removal of the leaf from the plant and then decreased rapidly over the next six weeks until the tenth week when the leaves themselves had disintegrated (Gauhl 1994). The survival of ascospores is directly related to the time it takes for the disintegration of the diseased leaf material (Stover 1980). Ascospores ejected are no longer viable after 6 hours of exposure to UV radiation (Parnell et al. 1998).
Spread of the Pathogen
Both M. musicola and M. fijiensis are dispersed within banana blocks by rain splash of conidia. Movement between blocks is possible through the aerial spread of ascospores ejected from the perithecia. Due to the larger amount of conidia produced by M. musicola than by M. fijiensis, conidia are considered the main means of spread for M. musicola while ascospores are the main method of dispersal of M. fijiensis (Stover and Dickson 1976).
Long distance spread may also be via the wind dispersal of ascospores. The short time that ejected ascospores can survive UV irradiation suggests that the distance viable ascospores are dispersed by this method will also be affected by the amount of cloud cover and the distance travelled through the night (Parnell et al. 1998). Recent population studies of both M.fijiensis (Rivas et al. 2004) and M. musicola (Hayden et al. 2005) however, suggest limited long distance dispersal-less than 50 m-of these pathogens based on the genetic structure of the populations. In many cases long distance movement, especially intercontinental movement, of the pathogen is thought to be more likely due to the direct transportation of germplasm from an infected area to a new region (Rivas et al. 2004).