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Prof. Edward (Ted) Farmer

Synopsis | Our past activities
 

Synopsis

The main question
There are approximately 600 gigatons of carbon in living vegetation on land. This carbon is a potentially valuable food source for animals, so why, wherever there is enough water on earth, is there so much plant mass? What mechanisms do plants use to protect their leaves ? Our research is aimed at understanding how organisms in the second trophic level (herbivores) try to sequester the carbon in leaves, organs that constitute a large part of the primary trophic level. We discovered that a signal transduction pathway, the jasmonate pathway, controls basal and inducible defense responses and this is now thought to limit carbon flow from plants to higher trophic levels.

Approach
The laboratory focusses on basic research aimed at understanding the regulation and evolution of the jasmonate pathway and of other lipid oxidation pathways. We use a broad range of methods.

Relevance
The range of leaves, fruits and seeds that are available to humans and their livestock is limited to a large extent by the same mechanisms that stop leaves being consumed by herbivores in nature. The question of how plants defend themselves from being eaten therefore has central relevance in ecology and in agriculture.

Areas in which we have published recently:

1. Activation of the jasmonate pathway in tissues distal to wounds requires electrical signals that are propagated by GLUTAMATE RECEPTOR-LIKE genes. Nature (2013) 500, 422-426.

2. The jasmonate pathway is structured differently in roots and aerial tissues (Proc. Natl. Acad. Sci. USA (2013) 110, 15473-15478.

3. The jasmonate pathway increases plant resistance to a vertebrate herbivore (Mol. Ecol. (2012) 21, 2534-2541).

4. Field observations from parts of the Americas, Asia, Africa and the Pacific have been integrated with results of laboratory experiments in : E.E. Farmer, Leaf Defence, Oxford University Press, 2014.


While jasmonates are made enzymatically from fatty acids, the membranes from which these fatty acids originate also undergo nonenzymatic oxidation. A second question we are addressing is : why is nonenzymatic lipid oxidation so prevalent when it is usually regarded as being deleterious ? We found that polyunsaturated fatty acids have roles as sinks for reactive oxygen species (ROS). That is, membrane lipids containing these fatty acids can now be regarded as structural antioxidants (J. Biol. Chem. (2009) 284, 1702; Ann. Rev. Plant Biol. (2013) 64, 429-450). This work is expected to provide evolutionary insights into lipid oxidation processes.
 

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Our past activities

Jasmonates

Proposed (with C.A. Ryan) a central role of jasmonates in the plant immune system (PNAS 87, 7713; Plant Cell 4, 129).

Performed the first experiments to investigate the effects of a signal transduction pathway on the feeding behavior of a vertebrate herbivore (Mol. Ecol. (2012) 21, 2534-2541).

Co-discovered (in parallel with the goups of J. Browse and R. Solano) members of the 'JAZ' family of repressor proteins and shown that a natural transcript from JAS1/JAZ10 plays a role in wound-induced growth inhbition. Also descibed the 'JAS' motif as a functional element in this protein (Plant Cell 19, 2470).

Discovered a new jasmonate (dnOPDA) and revealed a novel 'hexadecanoid' branch of the jasmonate biosynthetic pathway (PNAS 94, 10473).

We proposed that jasmonates can move through tissues to stimulate gene expression distal to wounds (Plant Physiol. 98, 995). However, a very different mobile signal is also involved (J. Biol. Chem. 284, 34506). We made the first constrained (minimum and maximum) velocity estimates for the speed of these long distance signals. We identified genes necessary for electrical signalling in plants (Nature 500, 422).

Showed that resistance to an insect can occur in the absence of wild-type jasmonic acid levels implicating cyclopentenone jasmonates (OPDA & dnOPDA) as signals (PNAS 98, 12837).

Proposed an integrative model for ethylene, salicylate and jasmonate action (Curr. Opin Plant Biol. 1, 404).

Quantitated (using microarrays and statistical analysis) the number of chewing insect-inducible genes that are regulated throught the jasmonate signal pathway (an estimated 67-84%) (Plant Cell 16, 3132) and shown that a specialist and a generalist insect activate this pathway almost equally.

Showed that jasmonate signalling promotes the establishment of a relatively oxidising environment near a wound (Plant Physiol. 156, 1797).

We isolated and characterized the 'fou2' mutant in the voltage-gated cation channel TPC1 from a genetic screen for plants with a constitutively active jasmonate pathway. This implicates cation flux (K+ and/or Ca2+) in the control over jasmonate biosynthesis (Plant J. 49, 889; Plant Cell Physiol. 2007, 48, 1775). Another mutant we isolated recently (fou8) suggests that sulphonucleotides (PAPS or PAP) help control JA levels in resting leaves.

 

Oxylipins control a major biological transition: from detritivory to herbivory

Evolution from detritivory (feeding on dead tissues) to herbivory (feeding on living plants) is one of the major transitions in biology. We starved isopod crustaceans (detritivores) and let them loose on Arabidopsis and rice mutants in jasmonate synthesis. The isopods started to feed on the living mutant plants but rarely damaged the WT (PNAS 2009, 106, 935). This shows that the absence of a signal pathway (the jasmonate pathway) in one organism causes a profound (transitional) effect on feeding in another.

 

Why do herbivores often cut round holes in leaves?

Now and again some of the things one finds changes the way one looks at nature. Herbivores often cut highly regular circles and semi-circles of leaf tissue. Birds often use the light coming through these holes to help them find caterpillars. In part the fact that insects often cut clean circles in leaves can be explained because it is simple and 'mechanically economic' (the insect doesn't have to move much) to do this. But there is more to the story. In carefully analysing microarray data we saw that some herbivores probably try to extract the maximum area of leaf tissue while leaving the minimal length of cut edge, so as to minimise stimulating plant defenses Plant Cell 12, 707). Insects understand calculus.

Missing phytoalexins from potato

Good candidates for low molecular mass antibiotics (phytoalexins) from the leaves of the historically and commercially important plant potato were unknown. They turned out to be relatively unstable molecules that had been described in vitro but that had previously escaped detection in living organisms. We identified divinyl ether fatty acids for the first time in nature in these leaves and proposed a role as antimicrobial compounds (Plant Cell 11, 485). They are the best candidates for the long-lost phytoalexins in potato leaves, the primary infection site for potato blight.

Antioxidant mechanisms

Antioxidants (such as tocopherols) and ROS-metabolising enzymes (such as catalase and SOD) are well established as controlling the overoxidation of cellular consituents. We propose that polyunsaturated fatty acids are used as 'ROS sinks' to literally soak up ROS (J. Biol. Chem. 2009, 284, 1702).

Reactive Electrophile Species (RES)

Proposed that 'reactive electrophile species' (RES) could play roles in abiotic stress responses and in the 'abiotic component' of biotic attack in plants (Plant J. 24, 467; Nature 411, 854). Developed a model for their beneficial and harmful actions in cells (Curr. Opin Plant Biol. 10, 380).

Demonstrated powerful biological activity in the ubiquitous and highly studied lipid peroxidation marker malondialdehyde (MDA) (Plant J. 37, 877) and showed that linolenic acid is the major source of damaging reactive molecules produced by non-enzymatic oxidation in plants (J. Biol. Chem. 202, 35749).

Developed a whole-body malodialdehyde mapping technique for the in situ visualization of MDA in complex organisms (J. Biol. Chem. 2007, 202, 35749) and discovered inducible pools of MDA in stem cell-rich tissues including the pericycle (J. Biol. Chem. 2012 in press).

Remorin: a new family of proteins

Discovered the remorin group of plasma membrane proteins. 'Remorins may be associated with the cytoskeleton or membrane skeleton i.e., in superstructures that help determine cell integrity and/or act as scaffolds for signaling in defense or development' (Plant Mol. Biol. 55, 579).

Community resources

Our laboratory has strongly supported the development of central, shared community resources in molecular biolgy and played a role in the establishment of the Lausanne DNA Array Facility.

 

 


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Biophore - CH-1015 Lausanne  - Switzerland  -  Phone +41 21 692 41 90  -  Fax  +41 21 692 41 95