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January, 2008
Source:
Proceedings of the National Academy of Sciences of the United
States of America
A guardian of grasses: Specific
origin and conservation of a unique disease-resistance gene in
the grass lineage
Anoop Sindhu, Satya Chintamanani, Amanda S. Brandt, Michael
Zanis, Steven R. Scofield, and Gurmukh S. Johal
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 (DR) gene
to be cloned, it remains a novelty because, instead of
participating in the plant recognition and response system as
most DR genes do, Hm1 disarms the pathogen directly. It does so
by encoding an NADPH-dependent reductase, whose function is to
inactivate Helminthosporium carbonum (HC) toxin, an
epoxide-containing cyclic tetrapeptide, which the pathogen
produces as a key virulence factor to colonize maize. Although
CCR1 is strictly a pathogen of maize, orthologs of Hm1 and the
HC-toxin reductase activity are present in the grass family,
suggesting an ancient and evolutionarily conserved role of this
DR trait in plants. Here, we provide proof for such a role by
demonstrating its involvement in nonhost resistance of barley to
CCR1. Barley leaves in which expression of the Hm1 homologue was
silenced became susceptible to infection by CCR1, but only if
the pathogen was able to produce HC toxin. Phylogenetic analysis
indicated that Hm1 evolved exclusively and early in the grass
lineage. Given the devastating ability of CCR1 to kill maize,
these findings imply that the evolution and/or geographical
distribution of grasses may have been constrained if Hm1 did not
emerge.
Open access article:
http://www.pnas.org/cgi/reprint/0711406105v1.pdf
RELATED RELEASE from
Purdue University
West Lafayette, Indiana
January 31, 2008
Gene
guards grain-producing grasses so people and animals can eat
Purdue University and
USDA-Agricultural Research Service scientists have discovered
that a type of gene in grain-producing plants halts infection by
a disease-causing fungus that can destroy crops vital for human
food supplies.
The research team is the first to show that the same biochemical
process protects an entire plant family - grasses - from the
devastating, fungal pathogen. The naturally occurring disease
resistance probably is responsible for the survival of grains
and other grasses over the past 60 million years.
The findings will stimulate the design of new resistance
strategies against additional diseases in grasses and other
plants. Grasses' ability to ward off pathogens is a major
concern because grasses, including corn, barley, rice, oats and
sorghum, provide most of the calories people consume, and some
species also increasingly are investigated for conversion into
energy.
A resistance gene, first discovered in corn, and the fungal
toxin-fighting enzyme it produces apparently provide a
biological mechanism that guards all grass species from this
fungus, said Guri Johal, a Purdue associate professor of botany
and plant pathology. He is senior and corresponding author of
the study published this week (Jan. 28-Feb. 1) in Early Edition,
the online version of the Proceedings of the National Academy of
Sciences. It will appear in the Feb. 5 print edition.
"We think that if the gene Hm1 had not evolved, then grasses
would have had a hard time surviving, thriving or, at least, the
geographic distribution would have been restricted," Johal said.
"This plant resistance gene is durable and is indispensible
against this fungal group, which has the ability to destroy any
part of the plant at any stage of development."
In 1943 a related fungus decimated rice crops in Bengal, causing
a catastrophic famine in which 5 million people starved. The
same fungal group was responsible for the other two recorded
epidemics in grasses in the 20th century, including the 1970
southern corn leaf blight that destroyed 15 percent of the U.S.
corn crop.
The study, part of an effort to prevent future crop crises, also
provides new information about the evolution of plant-pathogen
interaction, report Johal and his colleagues, including
USDA-Agricultural Research Service researcher Steven Scofield
and plant geneticist Michael Zanis. The findings have
implications for continued survival and further evolution of
grasses, which also include rye, bluegrass, reed canary grass
and bamboo.
Johal and the research team began this study because they had a
hunch that a genetic mechanism similar to the one protecting
corn from a fungus, called Cochliobolus carbonum race 1 (CCR1),
might also be at work in other grasses. They knew that all
grasses had genes similar, or homologous, to Hm1, but not
whether the same genetic mechanism was providing resistance
against the fungus and its toxin.
To determine if the same biochemical processes were at work to
prevent grass susceptibility to the fungus family, Johal and his
team shut off the Hm1 homologue in some barley plants. Next,
they infected the test barley with fungus.
In barley that no longer had a functioning Hm1 homologous gene,
the fungus, with the help of its toxin, caused disease in the
plant. The resulting tissue damage on the barley leaves was
typical of maize leaf blight symptoms in corn.
Some of the research barley, which had a functioning Hm1 gene,
was inoculated with the fungus. The results showed that the
resistance mechanism was the same as the one that prevents the
fungus' disease infection in corn.
As in corn, the Hm1-like gene produced an enzyme that disarmed
the fungus' disease-causing toxin. The detoxification isolated
the infection at the site where the fungus invaded. The research
with the barley also showed that, as in corn susceptible to the
fungus, infection isolation occurs if the fungus doesn't produce
the toxin.
Now that the researchers know that Hm1 homologues in all grasses
apparently trigger the same resistance to the fungal family, the
next step will be to investigate how the fungal toxin
facilitates disease when not degraded by Hm1.
Scofield is a scientist in the Purdue-based USDA-ARS Crop
Production and Pest Control Research Unit and a Purdue adjunct
assistant professor. Zanis is an assistant professor in the
Purdue Department of Botany and Plant Pathology. The other
researchers involved in the study were Anoop Sindhu, co-lead
author, former botany and plant pathology postdoctoral research
assistant and now an Iowa State University assistant scientist;
Satya Chintamanani, co-lead author and a postdoctoral research
assistant; and Amanda Brandt, a USDA-ARS research technician.
Purdue University, the National Science Foundation and the
USDA-Agricultural Research Service provided funding for this
research. |
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