Detoxification without intoxication: herbicide safeners activate plant defense gene expression.

Plants are frequently exposed to natural and synthetic toxins such as heavy metals, allelochemicals, organic pollutants, and pesticides. Consequently, plants must mount specific and coordinated defense mechanisms for survival under adverse growing conditions (Zhang et al., 2007). One such mechanism is the capability for metabolizing organic compounds from abiotic origin (xenobiotics). Extensive biotransformation is part of a strategy for coping with the potentially negative impacts of xenobiotics on plant growth and development. This is particularly evident in the capability for metabolic detoxification of herbicides; plants are able to detoxify herbicides by complex multistep processes that exhibit extraordinary diversity among species (Kreuz et al., 1996). The differential ability of plant species to metabolize a particular herbicide is widely exploited in modern agriculture by the use of selective herbicides that are safe to the crop but effectively control associated weeds. Another interesting feature of the herbicide detoxification system of some monocotyledonous crop species is inducibility by certain synthetic compounds collectively named “herbicide safeners.” Safeners are a group of chemically diverse compounds with the unique ability to protect grass crops from herbicide injury without reducing herbicide activity in target weed species (Davies and Caseley, 1999; Hatzios and Burgos, 2004). Safener protection from herbicide injury is accomplished by increasing the expression of genes encoding herbicide-metabolizing enzymes, such as the glutathione S-transferases (GSTs), cytochrome P450 monooxygenases (P450s), and several others (Hatzios, 1989; Farago et al., 1994; Riechers et al., 2005). Various safener chemical classes have been developed to enhance herbicide tolerance in maize (Zea mays), grain sorghum (Sorghum bicolor), rice (Oryza sativa), and small-grain cereals (Fig. 1). However, despite the widespread agronomic use of safeners for decades and ample information about their effects on increasing the activity of detoxification enzymes, there is virtually no knowledge of the molecular mechanisms for safener induction of their corresponding genes or signaling pathways being recruited. An exception is a safener-binding protein that was identified in maize, where its binding activity was characterized in maize seedlings (Walton and Casida, 1995) along with its gene expression patterns (Scott-Craig et al., 1998), although the precise role of this protein in the safenermediated signaling pathway has yet to be established. Safeners induce the expression of genes involved in plant defense and detoxification, such as GSTs and P450s, yet they are not toxic to the target plant and confer protection from herbicide injury. This suggests that safeners are tapping into an unidentified, preexisting signaling pathway for detoxification of endogenous toxins or xenobiotics (Riechers et al., 2005). A new hypothesis resulting from our most recent research is that safeners may be utilizing an oxidized lipid-mediated (oxylipins; Mosblech et al., 2009) or cyclopentenone-mediated signaling pathway, which subsequently leads to the expression of GSTs and other proteins involved in detoxification and plant defense (Weber, 2002; Loeffler et al., 2005; Mueller et al., 2008; Mueller and Berger, 2009). The goal of this Update on detoxification is to briefly review herbicide safener mechanism of action in light of the many recent findings related to oxylipins and their roles in signaling, induction of defense genes, and activation of detoxification responses in plants (Mueller et al., 2008; Mueller and Berger, 2009).