New insights from the Northern Leaf Spot disease of maize challenge
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New insights from the Northern Leaf Spot disease of maize challenge the prevailing views of adult plant resistance and the necrotrophic mode of fungal parasitism
Northern Leaf Spot disease of maize is caused by the fungus Cochliobolus carbonum race 1 (CCR1),
which employs a necrotrophic mode of growth to colonize its host. A key pathogenicity factor that CCR1 employs
to invade corn is HC-toxin, which confers on CCR1 the potential to decimate
corn of any age. Fortunately, a
resistance gene has evolved in maize that prevents CCR1 from causing
disease. Named Hm1, this resistance gene encodes an HC-toxin inactivating
reductase enzyme, HCTR, whose activity is dependent on NADPH as a
coenzyme. While the HCTR encoded by the
WT Hm1 protects maize at every stage
of development, the HCTRs encoded by the weak, partial loss-of-function alleles
of Hm1 do not. These mutant HCTRs confer disease resistance
only in mature plants, and not in young seedlings. The reason is that seedlings are not robust
enough metabolically to satisfy the heightened need of the cofactor NADPH for
the mutant HCTRs. Genes that confer
resistance only in adult tissues are called adult plant resistance (APR) genes,
and the resistance that they provide is believed to last for the remainder of
the life of the plant after onset.
However, our results with APR in the maize-CCR1 pathosystem are at odds with
this belief. While maize plants containing
the APR alleles turn as resistant as the plants containing the WT allele by
anthesis, they gradually become more and more susceptible afterwards during the
ear-fill period, and the severity of the disease relating inversely with the
HCTR activity of the APR allele. Thus,
APR in maize is dictated not by age but by the status of host metabolism.
We also explored the necrotrophic behavior of CCR1 to accomplish host invasion. All necrotrophic pathogens are thought to have the potential to cause disease by taking advantage of any kind of cell death in the host. This includes cell death that accompanies the hypersensitive immune response (HR), as has been witnessed with Botrytis and C. victoriae in Arabidopsis. Interestingly, this was not the case with CCR1. CCR1 was not able to colonize maize cells dying from HR in an autoimmune mutant, provided the functional Hm1 gene was in the background. These results suggest that not all necrotrophic pathogens are created equal, as has been presumed all along. My results clearly suggest that while some necrotrophs are able to take advantage of the HR cell death for host colonization, others do not.
Another result of key interest is that the HR cell death and the associated induction of the defense response also did not alter the outcome of the susceptible reaction of maize to CCR1. Susceptible plants with the genotype hm1hm1 were equally susceptible to CCR1 regardless of whether the plants carried the autoimmune gene Rp1-D21 or not. These findings imply that HC-toxin does not induce host susceptibility by interfering with the induction of defense responses, as has been acclaimed.