Submitted to: Journal of the National Academy of Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/10/2008
Publication Date: 3/17/2008
Citation: Sindhu, A., Chintamanani, S., Scofield, S.R., Brandt, A.S., Johal, G. 2008. A guardian of grasses: specific origin and conservation of a unique disease-resistance gene in the grass lineage. Journal of the National Academy of Sciences. 105:1762-1767. Interpretive Summary: The Hm1 disease resistance gene provides protection against race 1 of Cochliobolus carbonum, which causes a severe leaf blight and ear mold disease in maize. It (Hm1) does so by inactivating HC-toxin, a key determinant of this disease. Hm1 is conserved among cereals, which raised the possibility that it is derived from a common ancestor. To test if Hm1 could serve a similar function in other grasses, we used VIGS to assay its function in barley which is not susceptible to C. carbonum race 1. Our results clearly demonstrate that resistance of barley to the HC-toxin-producing isolates of C. carbonum is lost in leaves in which the Hm1 homolog(s) has been silenced. A key implication of this finding is that HC-toxin has the ability to impair host defenses in all cereals. Another implication of this study is that it demonstrates that the non host resistance of barley is due to an active mechanism conferred by the Hm1 gene. This work has also an important evolutionary implication for the survival and evolution of the grass lineage (if not the entire monocot class).
Technical Abstract: The maize Hm1 gene provides protection against a lethal leaf blight and ear mold disease caused by Cochliobolus carbonum race 1 (CCR1). Although it was the first disease resistance (R) gene to be cloned in plants, it remains a novelty because instead of participating in plant’s recognition and response system, as most R genes do, Hm1 disarms the pathogen directly. It does so by encoding HCTR, whose function is to inactivate HC-toxin, an epoxide-containing cyclic tetrapeptide, which the pathogen needs to colonize maize. While CCR1 is strictly a pathogen of maize, orthologs of Hm1 as well as the HCTR activity are present widely in the grass family, suggesting an ancient origin and recruitment of this disease resistance trait in the grass lineage. Here we provide proof for its role in plant protection since antiquity, and show that the nonhost resistance of barley to CCR1 is conferred by HCTR. Barley leaves in which expression of the Hm1 homologs was silenced became susceptible to infection by CCR1, but only if the pathogen was able to produce HC-toxin. Given that CCR1 is a devastating pathogen capable of decimating maize, one sobering implication of this revelation is: What would have happened to cereals, the major source of food for the humankind, if Hm1 did not exist?