The Plant Cell, Vol. 28: 1001, May 2016, www.plantcell.org ã 2016 American Society of Plant Biologists. All rights reserved.
IN BRIEF
Opposing Functions for Plant Xanthine Dehydrogenase in Response
to Powdery Mildew Infection: Production and Scavenging of
Reactive Oxygen Species
OPEN
Xanthine dehydrogenases are fascinating
enzymes. Their basic function is in purine
catabolism, catalyzing the conversion of hypoxanthine to xanthine and xanthine to uric
acid. In mammals, xanthine dehydrogenases,
which use NAD1 as electron acceptor to produce uric acid, can be posttranslationally
modified to become xanthine oxidases, which
use O2 as electron acceptor to produce reactive oxygen species (ROS). Because uric
acid is a scavenger of ROS, the resulting influence of xanthine dehydrogenase on ROS
status is likely responsible for its importance
in a remarkably wide range of processes
in mammals, including immunity (reviewed in
Vorbach et al., 2003). Plant xanthine dehydrogenases, like those of chicken and Drosophila
melanogaster, have not been reported to undergo an analogous posttranslational modification, but do appear capable of using both O2
and NAD1 as electron acceptors, as well as of
producing high levels of ROS (Zarepour et al.,
2010). Now, Ma et al. (2016) report that
xanthine dehydrogenase is important in
defense responses in Arabidopsis thaliana,
likely through roles in both production of
ROS in epidermal cells and scavenging of
ROS in mesophyll cells.
The powdery mildew fungus Golovinomyces
cichoracearum triggers defense responses in
Arabidopsis mediated by the R gene RPW8.2.
In a screen for mutants defective in RPW8.2related resistance to powdery mildew, Ma and
coworkers identified three plants with point
mutations in XANTHINE DEHYDROGENASE1
(XDH1), including two that altered residues
strictly conserved among xanthine dehydrogenases. The mutants showed impaired resistance to powdery mildew and accumulated
less H2O2 in the haustorial complex in epidermal cells invaded by the fungus. These point
mutations decreased the activity of recombinant XDH1 proteins, in terms of both dehydrogenase activity and ROS production.
OPEN
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Thus, XDH1 activity appears to be important for RPW8.2-mediated powdery mildew
resistance.
Interestingly, the authors observed autofluorescent objects (AFOs) within mesophyll
cells of the mutant plants. The AFOs were
highly enriched in xanthine, and the authors
cleverly used AFO formation as a marker for
xanthine accumulation with both spatial and
temporal resolution. They found that xanthine
accumulation in the mutants was further induced by pathogen inoculation, suggesting
that there is increased purine catabolism
(mediated at least in part by XDH1) upon
infection. Importantly, the authors observed
both local and systemic induction of AFOs
(i.e., purine catabolism) in response to powdery mildew infection. This finding supports
the authors’ conclusion that upregulation
of purine catabolism is part of the defense
response.
Cell death during the hypersensitive response is generally preceded by production
of ROS and is often confined to site of infection. Ma et al. propose that plants spatially constrain the hypersensitive response
by upregulating purine catabolism to produce uric acid (via XDH1 activity) as a ROS
scavenger. Indeed, the authors found that
feeding uric acid suppressed the H2O2 accumulation normally observed in mesophyll
cells of infected xdh1 mutant plants. Together, the data in this work support a model
in which XDH1 in epidermal cells contributes
to the ROS burst to help restrict the area of
fungal infection while XDH1 in underlying
mesophyll cells serves to protect chloroplasts from oxidative damage by producing
ROS scavengers (see figure). Thus, XDH1
appears to be an important tool allowing
plants to harness and direct the power of
ROS.
Nancy R. Hofmann
Science Editor
[email protected]
ORCID ID: 0000-0001-9504-1152
XDH1 plays opposing roles to harness ROS in
resistance to powdery mildew fungus. In invaded
epidermal cells, XDH1 produces superoxide, contributing to the ROS burst that constrains the fungal
haustorium. In mesophyll cells, XDH1 produces uric
acid to scavenge ROS and protect chloroplasts
from oxidative damage. (Adapted from Figure 9 of
Ma et al. [2016].)
REFERENCES
Ma, X., et al. (2016) Dual and opposing roles of
xanthine dehydrogenase in defense-associated
reactive oxygen species metabolism in Arabidopsis. Plant Cell 28: 1108–1126.
Vorbach, C., Harrison, R., and Capecchi, M.R.
(2003). Xanthine oxidoreductase is central
to the evolution and function of the innate
immune system. Trends Immunol. 24: 512–
517.
Zarepour, M., Kaspari, K., Stagge, S., Rethmeier,
R., Mendel, R.R., and Bittner, F. (2010). Xanthine
dehydrogenase AtXDH1 from Arabidopsis thaliana
is a potent producer of superoxide anions via its
NADH oxidase activity. Plant Mol. Biol. 72: 301–
310.
Opposing Functions for Plant Xanthine Dehydrogenase in Response to Powdery Mildew Infection:
Production and Scavenging of Reactive Oxygen Species
Nancy R. Hofmann
Plant Cell 2016;28;1001; originally published online May 10, 2016;
DOI 10.1105/tpc.16.00381
This information is current as of July 31, 2017
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References
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