 his
month, in-cites talks with Professor Chris Lamb about his
paper, "The oxidative burst in plant disease
resistance," (Lamb C and Dixon RA, Annu. Rev. Plant
Physiol. Plant Mol. Biol. 48: 251-75, 19971).
According to Essential
Science Indicators ,
this paper currently ranks #2 among Plant & Animal Science
papers published over the past decade, with 810 citations.
Professor Lamb’s record in this field includes 34 papers
cited a total of 3,134 citations to date. Professor Lamb is
the Director of the John Innes Centre and is the John Innes
Professor of Biology at the University of East Anglia.
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Would you give us some
background on your education and research
interests?
My B.A. and Ph.D. were in biochemistry, both from Cambridge. I
was a post-doctoral fellow and then junior faculty member at Oxford
before moving to California in 1982 to start a plant biology program
at the Salk Institute. My initial interests were in the regulation
of plant natural product biosynthesis, and in 1978 I started
collaborating with Richard Dixon, bringing together a cell culture
system he had developed and a technique I had refined to look at the
synthesis and turnover of specific plant enzymes. This led to
molecular cloning of genes encoding key enzymes of plant natural
products involved in protection against pathogen attack and the
demonstration of a spatial and temporal hierarchy for activation of
defense-related genes earlier or more effectively in a resistant
than a susceptible plant.
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“The oxidative burst has been implicated in making the whole plant more refractory to further attacks by pathogens, and we are combining genetics and physiology to dissect key distinctive features of this broad-spectrum-acquired resistance as well as the underlying basal resistance (disease limitation) mechanisms.”
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My lab started working on the oxidative burst in the early ‘90s
as the result of an unexpected observation made while looking for
events at the plant cell surface potentially involved in perception
and relay of pathogen signals for defense gene activation. Noriyuki
Doke’s lab at Nagoya had reported that plants attacked by
pathogens or stimulated by pathogen-derived signal molecules
(elicitors) underwent an oxidative burst similar to that in
activated neutrophils.
However, possible functions of the
plant oxidative burst were unclear and for a while it remained
something of a curiosity. While studying early elicitor-induced
changes at the plasma membrane, Des Bradley and Per Kjellbom noted the
extremely rapid apparent disappearance of two abundant proline- and
tyrosine-rich proteins in another compartment—the cell wall2.
On further investigation this turned out not to reflect degradation of
the proteins but their rapid insolubulization by oxidative
cross-linking driven by the oxidative burst. Such cross-linking
provided a rapid toughening of the cell wall, making it more
refractory to pathogen ingress while transcription-dependent defenses
were activated and deployed.
These findings prompted us, in collaboration with Richard’s lab,
now at the Noble Foundation in Oklahoma, to look for other functions
of the pathogen-induced oxidative burst. In particular, Alex Levine
and Raimund Tenhaken were able to show that reactive oxygen
intermediates (ROI) functioned as signals for activation of subsets of
defense genes and at higher levels triggered the programmed host cell
death that underlies the development of a restricted hypersensitive
lesion at the site of attempt ed
attack3.
Would you please sum up the key points of your 1997 review of
oxidative burst in plant disease resistance?
It was nice to be invited to write an Annual Review
article about an area of research that was relatively new for us.
The review summarized the biology first established by Doke and the
recent findings on function. We also reviewed the underlying
biochemistry of the generation and inter-conversion of ROI, and
possible mechanisms for the generation of these species in the
oxidative burst and how they might trigger downstream responses.
Where has research into oxidative burst gone since this review?
I suppose the review has been highly cited because research on
the oxidative burst in plant-pathogen interactions has remained very
active and the oxidative burst has been shown to be involved in
other biological processes. A number of mechanisms contributing to
the oxidative burst have been identified and characterized in
molecular detail. One of the main mechanisms turns out to be by
activation of homologues of the neutrophil NAPDH oxidase but with
fascinating differences in the regulation of the enzyme. There is a
less complete story on how ROI exert their signal functions,
although modulation of calcium channels appears to be a central
feature. More surprisingly, ROI have been implicated as signal
molecules or effectors in a wide range of other biological
processes.
The early work by Des and Per indicated that oxidative
cross-linking could also be induced by wounding in the absence of
pathogen, and Bud Ryan’s group at Pullman has shown that ROI are
important signals in plant-herbivore interactions. However, it is
now clear that ROI also function as signals of abiotic stress and in
plant development, e.g., growth of root hairs. This raises obvious
questions about specificity of output and possible co-signals. For
example, Massimo Delledonne showed that nitric oxide functions as a
co-signal with ROI to trigger a strong hypersensitive cell death
response with NO independently regulating another subset of defense
genes.
Has the study of oxidative burst resulted in any practical
applications?
A number of strategies involving transgenic manipulation to
enhance or pre-induce the accumulation of ROI have been shown to
promote disease resistance under glasshouse conditions. However,
there would potentially be issues regarding costs of such
resistance, unless deployment was carefully poised, and I am not
aware of any such strategies having been taken through to
commercialization. At a recent meeting in Budapest, I heard about a
clever approach by Zoltan Kiraly and colleagues to use low-level
enhancement of ROI levels to reduce symptom development and economic
damage in fruit crops.
If you are free to talk about them, what are your current projects?
When I became Director of the John Innes Centre in 1999 I wished
to retain an active lab but agreed it should be smaller than in the
past. I have focused on long-distance signaling of pathogen attack.
The oxidative burst has been implicated in making the whole plant
more refractory to further attacks by pathogens, and we are
combining genetics and physiology to dissect key distinctive
features of this broad-spectrum-acquired resistance as well as the
underlying basal resistance (disease limitation) mechanisms. We are
increasingly taking an integrative approach including studies on the
costs of such resistances to the plant and understanding the
interplay between biotic and abiotic stress signaling and between
stress responses and metabolism.
Professor Chris Lamb
John Innes Centre
Norfolk, UK
- The oxidative burst in plant disease resistance. Cited 832 times [Web of Science 6.11.06].
- Bradley, D.J., Kjellbom, P. and Lamb, C.J. (1992) Elicitor-induced and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70: 21-30. Cited 593 times.
- Levine, A., Tenhaken, R. Dixon, R.A. and Lamb, C. (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593. Cited 1127 times.
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