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Growth Regulation and Other Secondary Effects of Herbicides Edivaldo D Weed Science 2010 58:351–354 Growth Regulation and Other Secondary Effects of Herbicides Edivaldo D. Velini, Maria L. B. Trindade, Luis Rodrigo M. Barberis, and Stephen O. Duke* As all herbicides act on pathways or processes crucial to plants, in an inhibitory or stimulatory way, low doses of any herbicide might be used to beneficially modulate plant growth, development, or composition. Glyphosate, the most used herbicide in the world, is widely applied at low rates to ripen sugarcane. Low rates of glyphosate also can stimulate plant growth (this effect is called hormesis). When applied at recommended rates for weed control, glyphosate can inhibit rust diseases in glyphosate-resistant wheat and soybean. Fluridone blocks carotenoid biosynthesis by inhibition of phytoene desaturase and is effective in reducing the production of abscisic acid in drought-stressed plants. Among the acetolactate synthase inhibitors, sulfometuron-methyl is widely used to ripen sugarcane and imidazolinones can be used to suppress turf species growth. The application of protoporphyrinogen oxidase inhibitors can trigger plant defenses against pathogens. Glufosinate, a glutamine synthetase inhibitor, is also known to improve the control of plant diseases. Auxin agonists (i.e., dicamba and 2,4-D) are effective, low-cost plant growth regulators. Currently, auxin agonists are still used in tissue cultures to induce somatic embryogenesis and to control fruit ripening, to reduce drop of fruits, to enlarge fruit size, or to extend the harvest period in citrus orchards. At low doses, triazine herbicides stimulate growth through beneficial effects on nitrogen metabolism and through auxin-like effects. Thus, sublethal doses of several herbicides have applications other than weed control. Nomenclature: 2,4-D; dicamba; fluridone; glyphosate; imazpic; lactofen; simazine; sulfometuron-methyl; soybean, Glycine max (L.) Merr.; sugarcane, Saccharum spontaneum L.; wheat, Triticum aestivum L. Key words: Growth regulation, herbicide, hormesis, secondary effects. Most herbicides are compounds that inhibit plant the world. This herbicide is an essential tool for developing metabolic pathways or physiological processes by interacting sustainable production systems, and in the last years its with specific proteins (Dayan et al. 2010). As a consequence consumption has increased continuously because of the of the inhibition, plants will die or stop growing. The auxin development of glyphosate-resistant crop varieties (Duke agonists are exceptions as they promote auxin-mediated and Powles 2008). Glyphosate is also widely used to control effects, resulting in uncontrolled growth in plants. As all undesired plants in noncrop areas like roads, railways, and herbicides act on pathways or processes crucial to plants, as water bodies. inhibitors or stimulators, possibly low doses of any herbicide Glyphosate is the only commercially available herbicide can modify plant growth, development, or composition in inhibiting the enzyme 5-enolpyruvyl-shikimate-3-phosphate ways that might be beneficial under some circumstances. synthase (EPSPS), blocking the synthesis of aromatic amino There are several theoretical ways by which plants can have acids and secondary compounds derived from these amino contact with low rates of herbicides, including unwanted drift acids (Duke 1988). Several compounds produced from deposition, accidental application to the crop in sprays directed aromatic amino acids are involved with growth regulation, at the weeds, contact of the crop leaves with treated weeds, wood quality, allelopathic effects, and resistance to pests and protection by taller plants reducing the number of droplets that diseases. Some examples of these compounds are indolacetic can reach a weed, and absorption of low doses from the soil. acid, lignin, salicylic acid, methyl salicylic acid, and stilbenes Herbicides also can be applied at low doses as a consequence of (Velini et al. 2009). the lateral and vertical movements of the nozzle boom and the Most plant species are sensitive to glyphosate. Plants treated covering by crops, weeds, or mulch (Gazziero et al. 2006; Souza with glyphosate accumulate high levels of shikimate (Amrhein et et al. 2007). Because of nozzle boom movements, some plants al. 1980, 1981; Becerril et al. 1989; Burke et al. 2005; Duke can also receive rates much higher than average. 1988; Harring et al. 1998; Singh and Shaner 1998; Velini et al. Herbicides also can intentionally be applied to crops at low 2008). This herbicide can be useful to raise shikimate content in rates, aiming at growth regulation, the modification of plant plants as shikimic acid is one of several industrially interesting biomass composition, or the accumulation of specific chiral starting materials formed in the aromatic amino acid compounds. Herbicides inhibiting complex biosynthetic pathway of plants (Johansson et al. 2005), as it is a precursor for processes like carotenoid, lipid, and amino acid synthesis semisynthesis of oseltamivir (Enserink 2006), an antiviral drug pathways are good candidates for the uses mentioned above as used to control nonresistant strains of the influenza virus. There their application can change the concentrations of many has been a worldwide shortage of shikimate, and glyphosate compounds or classes of compounds in plants. could be used to enhance production in species such as star anise (Illicium verum Hook. f.), one source from which it is Secondary Effects of Glyphosate commercially extracted. EPSPS is not exclusive to plants. It is a key enzyme in the Glyphosate (N-phosphonomethylglycine) is extensively synthesis of aromatic amino acids in plants, bacteria, and used to control weeds in annual and perennial crops all over fungi (Feng et al. 2005; Kishore and Shah 1998). Several authors have reported effective rust control after glyphosate DOI: 10.1614/WS-D-09-00028.1 application to soybean and wheat resistant to glyphosate * First, second, and third authors: UNESP—Universidade Estadual, College of Agronomic Sciences, Botucatu, Brazil; fourth author: USDA-ARS, Natural under field conditions (Anderson and Kolmer 2005; Feng et Products Utilization Research Unit, P.O. Box 8048, University, MS 38677. al. 2005, 2008; Soares et al. 2008). As glyphosate can affect Corresponding author’s E-mail: [email protected] plants and pathogens, its effects on disease severity is not Velini et al.: Secondary effects of herbicides N 351 uniform. Whereas the inhibition to pathogens and diseases Secondary Effects of Acetolactate Synthase has been frequently reported, the severity of some diseases was (ALS) Inhibitors not affected or was increased by glyphosate (Duke et al. 2007b; Sanyal and Shrestha 2008). Although glyphosate is Sulfometuron-methyl has been widely used at rates ranging fungicidal and bactericidal to some plant pathogens, in from 10–20 g ha21 to ripen sugarcane (Castro 1999, 2000; nonglyphosate-resistant plants glyphosate can reduce phyto- Castro et al. 1996, 2009). This herbicide can be used alone or alexin levels, making the plant more susceptible to the mixed with glyphosate. pathogen (Keen et al. 1982; Sharon et al. 1992). Thus, in Among the ALS inhibitors, imazapic (Gover et al. 2004; nonglyphosate-resistant crops the effect of glyphosate on Hixson et al. 2007), imazamethabenz (Yelverton et al. 1997), disease virulence is a balance between the relative effect of and chlorsulfuron (Hixson et al. 2007) were effective to glyphosate on the plant vs. the pathogen. Most of the reduce turf growth to reduce frequency of mowing. Imazapic literature suggests that the pathogen wins this contest. But, in provided season-long seedhead suppression in bahiagrass glyphosate-resistant crops, there is growing evidence that the (Paspalum notatum Fluegge´) but rates over 71 g ha21 reduced crop may benefit from glyphosate application in its battle plant density (Yelverton et al. 1997). When sprayed to tall against some pathogens. These interactions deserve further fescue [Lolium arundinaceum (Schreb.) S.J. Darbyshire] at study. rates ranging from 9 to 53 g ha21, imazapic suppressed new Glyphosate applied at low rates can increase plant growth. vegetative growth and seedhead for 3 mo (Hixon et al. 2007). The stimulatory effect of subtoxic doses of a toxicant is called hormesis and has been reported for low doses of many Secondary Effects of Protoporphyinogen IX herbicides on plants including glyphosate (Cedergreen et al. 2007; Duke et al. 2007a; Schabenberger et al. 1999; Velini et Oxidase Inhibitors al. 2008; Wagner et al. 2003). Sublethal doses of glyphosate The protoporphyrinogen IX oxidase enzyme, known as stimulate growth of a range of plant species, and hormesis is Protox or PPO, corresponds to the site of action of several likely to be related to the molecular target of glyphosate, since herbicides from different chemical groups. The herbicide the effect was not seen in glyphosate-resistant plants (Velini et action is implicated in promoting oxidative stress by al. 2008). Low doses of glyphosate are not recommended as a producing free radicals (Dayan and Duke 1997). Mild growth stimulant for crops, as the hormetic dose could vary oxidative stress is known to induce plant defenses against considerably depending on many factors, including climate, pathogens, including elicitation of the synthesis of phytoalex- plant variety, plant developmental stage, and glyphosate ins. The potential effects of Protox inhibitors to raise plant formulation. defenses against plant pathogens was
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