Inheritance and mechanisms of resistance of Sorghum (Sorghum bicolor) to Sorghum Ergot (caused by Claviceps africana)

Abstract

Worldwide, ergot of grain sorghum (Sorghum bicolor) is caused by three species of Claviceps, of which C. africana is the most widespread. From an initially limited distribution in Africa, C. africana swept across the globe through the 1990's, and was first recorded in Australia in 1996. Ergot remains an important pathogen, as the toxic effects of the ergot alkaloids (reported only from Australia) impact on the entire sorghum production chain. Ergot also increases the cost of grain and hybrid seed production. C. africana infects unfertilised florets, replacing the developing ovary with a fungal mass. After colonising the ovary, the fungus secretes a sticky honeydew (containing macroconidia). Airborne secondary conidia are produced from macroconidia germinating near the honeydew surface, and are the source of widespread epidemics. A successfully fertilised ovary is resistant to ergot infection (known as 'escape resistance'), so environmental factors that reduce the availability or viability of pollen can result in greater ergot infection.Current commercial sorghum cultivars have no resistance to C. africana. An African land-race of S. bicolor, IS8525, was found to express ergot resistance in Australia, yet nothing was known of the genetic nature of the resistance, what the most efficient breeding system might be to capture the resistance, or why it was resistant.The inheritance of resistance to sorghum ergot from IS8525 was determined. Ergot severity, and pollen trait data were collected from populations of IS8525 crossed with the elite inbred-lines 31945-2-2 and 60535-2-2. Narrow-sense heritability for ergot resistance was high (0.78 and 0.62 respectively for the two studied populations), and a simple additive-dominance model explained the genetic control of this character (maternal or epistatic effects were not detected). There may be as few as two genes controlling ergot resistance in IS8525 (as estimated biometrically). Additivedominance effects were estimated at a range of time points, showing that estimates fluctuated with environmental conditions. Different genetic parameter estimates were found under differing disease pressures, with dominance effects harder to detect when disease pressure was low, highlighting the strength of the environmental influence. Pollen traits (pollen viability and pollen quantity) had a low heritability. Dominance genetic effects influenced pollen viability more than additive genetic effects or the environment, meaning that this pollen trait will not respond to selection. Pollen quantity was influenced by non-genetic (environmental) variation, rather than genetic effects, resulting in a low heritability estimate (0.37) from the IS8525/60535-2-2 population; no heritability estimate was possible from the other population. These findings mean that successful breeding for ergot resistance can be conducted with a reduced screening population size and using simpler breeding methods (such as backcross breeding), thereby enabling quicker release of ergot-resistant germplasm. Breeding for ergot resistance, based on IS8525, will not influence the pollen traits.In experiments designed to determine the resistance mechanism(s), susceptible genotypes were found to take significantly longer than IS8525 to complete flowering, exposing the ovary to the atmosphere for a longer time period. Were ergot conidia directly infecting the ovary during flowering? My results suggest this may be the case. This hypothesis was tested by inoculating the ovary during flowering, and the stigma after flowering had stopped, using both fertile spikelets and emasculated spikelets. Without pollen, IS8525 has no ergot resistance. Inoculating the ovary removed the resistance effect gained through pollen. The response to pollen was not unique to IS8525, being also found in susceptible genotypes.This suggests that a longer flowering duration in susceptible genotypes is related to greater access to the ovary infection site by airborne conidia. The shorter flowering duration of resistant genotypes acts to shield the ovary from aerial conidia, in combination with the natural senescence response to pollen which closes the stigma/style pathway of infection.A number of other potential resistance mechanisms were also tested and found to be unrelated to ergot resistance. These included the role of stigma receptivity to ergot conidia, stigma morphology, and the possibility of resistance based on avoidance of airborne conidia through the timing of flowering.