Understanding herbicide hormesis: Evaluating its positive and negative aspects with emphasis on glyphosate

Abstract

Research on the uses of herbicide hormesis to improve crop yield and the role of herbicide hormesis in weed management has greatly increased in recent years. The use of herbicide hormesis to improve crop quality and yield has been hampered by erratic results and difficulty in choosing a dose that will provide reliable hormesis in the field. A sequential application of low glyphosate doses in the form of a seed treatment followed by a low dose after seedling emergence has been recently shown to provide more predictable hormesis in the field, resulting in significant increases in crop yield. However, herbicide hormesis can hamper weed management with herbicides in two ways. Recommended herbicide doses that overlap the hormetic dose range of some weeds can give them a competitive advantage. This is probably rare, but hormesis for weed subpopulations that are more tolerant/resistant than most of the plants in a weed population can accelerate the selection for and spread of herbicide resistance, a potentially more common phenomenon. The molecular mechanism(s) of herbicide hormesis is/are still unknown, other than mild stress triggering overcompensation, resulting in enhanced growth and reproductive processes. Glyphosate hormesis appears to be more consistent and pronounced than that with other herbicides. This may be due to large number of essential compounds produced by the shikimic pathway, compared to other herbicides and/or to its highly systemic mode of action.

Growth Stimulation; Lignin; Mode of Action; Shikimate

1.Introduction

Hormesis is the stimulatory effect of a subtoxic concentration or dose of a chemical compound that is toxic at higher doses (Calabrese et al., 2007). Hormesis is observed with both chemical and other stresses in all types of organisms and has been a controversial topic in toxicology. Pesticide-induced hormesis is observed in insects and fungi with low doses of insecticides (Cutler, Guedes, 2017) and fungicides (Pradhan et al., 2017), respectively. This phenomenon has also been observed in responses of plants to low herbicide doses for many years, and numerous papers have been published on the topic. Herbicide hormesis is more than just a scientific curiosity, as there is potential to use it to improve crop production, and it may play a role in the growing problems of evolution and spread of herbicide-resistant weeds. The topic of herbicide-caused hormesis has been reviewed in recent years (e.g., Belz et al., 2011; Belz, Duke, 2014; 2017; Brito et al., 2018; Jalal et al., 2021).

The volume of literature on herbicide hormesis has increased exponentially over the last 65 years (Figure 1). The number of papers on herbicide hormesis shown in Figure 1 is an underestimate, as there are many papers, particularly older ones, that describe herbicide hormesis without using the term hormesis (e.g., Wiedman, Appleby, 1972). In earlier papers, terms such as ‘growth stimulation’ were used. Previously reviewed literature is not discussed in detail in this perspective, as well as the modelling of this dose-response phenomenon (for modelling see e.g. Cedergreen et al., 2005 or Belz, Duke, 2022a). The objective of this review is to provide an update on what we consider the most important recent findings and insights into utilization of herbicide hormesis to improve crop quality and yield, the potential influences of herbicide hormesis on weed management, especially on evolution and spread of herbicide resistance, and the mechanism(s) of herbicide-induced hormesis.

Figure 1
Publications on hormesis and herbicides over the past 65 years compiled form Google Scholar in late 2024 using the keyword combination of herbicide and hormesis. Each histogram bar represents the number of publications from the previous 10 years

2.Using herbicide hormesis to improve crop quality and yield

Low-dose stressors can enhance plant health and yield (Agathokleous et al., 2024). A major reason for the growing interest in herbicide hormesis is the promise of using this phenomenon to improve crop quality and/or yield. A long history exists of scientists attempting to use subtoxic levels of herbicides for this purpose. Patents exist for the utilization of low doses of glufosinate (Donn, 1998), glyphosate (Brants, Graham, 2000), and acetolactate synthase inhibitor herbicides (McGregor et al., 2015) to increase crop yields. Herbicide hormesis to improve crop production has been previously reviewed (Belz et al., 2011), so we will give only a few examples of older research on this topic.

There were early attempts to use subtoxic herbicide doses to improve crop quality, such as the use of triazine herbicides to improve protein content of crops (e.g., Ries et al., 1967). Despite excitement about this work, no practical use of this knowledge was developed. Early work by Weidman and Appleby (1972) found herbicides with several modes of action (inhibitors of PSII and very long chain fatty acid synthesis, interference with tubulin polymerization, and auxin mimics) to increase plant growth. The late Arnold Appleby stated in a personal conversation with one of us (SOD) in 2006 that inconsistent field results caused him to abandon attempts to use low herbicide doses to improve crop quality and/or yields. Subsequent research has confirmed extreme variability as to whether hormesis occurs at all or the degree to which it occurs in the field or even in the greenhouse, due to many environmental variables that affect the growth status of the plant (e.g., light, temperature, soil nutrients, exposure to other chemicals, plant density, CO₂ concentration., etc.) (reviewed in Belz et al., 2011; Belz, Duke, 2022b). Furthermore, the time after the low herbicide dose is administered is important, as it takes time for hormesis to develop, and it can disappear after it has appeared (Belz et al., 2011). Generalizing, hormesis is most likely in crop physiological ranges dictated by certain environmental conditions (e.g., nutrient concentration) that are suboptimal and/or are in an environmental range (e.g., temperature) that potentially allows good growth (Belz, Duke, 2022b).

Most papers on the effects of hormesis on crops do not determine the effects on harvestable yield in the field (e.g., Ferrari et al., 2021). Determining the proper dose and time of application to get such a desirable effect is problematic, considering the variable and ever-changing environmental parameters in the field. For crops with which biomass of the leaves and stems are harvested (e.g., fodder crops, sugarcane), obtaining increased yields might be simpler. There are many more papers in which the biomass of plant parts is increased by low herbicide doses than those demonstrating an increase in harvested grain, seeds or fruit. For example, Codognoto et al. (2023) reported that sequential applications of 5.4 and 10.8 g ae per ha^-1 of glyphosate increased the yield of three cultivars of the forage grass genus Urochloa. Even rarer are hormesis studies that determine the impact on qualitative yield parameters. Nevertheless, papers continue to be published in which low doses of herbicides, particularly glyphosate, cause increases in crop yield of harvested grain. Some recent examples are yield of white oat (Avena sativa L.) grain being increased 30% by low glyphosate doses under low nitrogen availability (Silva et al., 2020a), and yield of common bean (Phaseolus vulgaris L.) seed being increased by 21% by 11 g ae ha^-1 glyphosate, again under low nitrogen availability (Silva et al., 2020b). In another study with common bean, 7.2 g ae ha^-1 glyphosate produced a 23% yield increase in grain yield and 36 g ae ha^-1 glyphosate caused a 111% yield increase (Bortolheiro et al., 2023). An increase in yield of wheat by 30% with 18 g ae ha^-1 glyphosate was found by Abbas et al. (2016), and a 34% increase in yield of chickpea (Cicer arietinum L.) was caused by 7.2 g ae ha^-1 glyphosate (Abbas et al., 2015). Low doses of 2,4-D have been reported to increase cotton yield (Aguilar et al., 2021).

Even though patents exist for the use of herbicides with at least three modes of action for increasing crop yield, the only method for the use of low herbicide doses of which we are aware that farmers use routinely is that of low glyphosate doses to increase sugar content of sugarcane (Saccharum spp.) at harvest time (Dalley, Richard, 2010; Carbonari et al., 2014; Pincelli-Soiuza et al., 2020). This effect may be partly due to glyphosate being translocated to metabolic sinks (Duke, 2020), such as meristems, and thereby reducing utilization of sucrose by developing tissues, resulting in higher levels of sucrose accumulating in harvested stem tissue. Other herbicides that have the same effects (reducing sucrose translocation to metabolic sinks), such as fluazifop and sulfometuron-methyl, have also been used to increase sucrose in sugarcane (Dalley, Richard, 2010).

Considering the extensive research on herbicide hormesis in crops, the lack of other cases of low herbicide doses being recommended for enhanced yield or crop quality, other than on sugarcane, is surprising. However, the many papers with positive results may not be an accurate representation of all research on this topic, as positive results are generally much more likely to be accepted for publication than negative results. The many variables in field settings that can influence herbicide hormesis make the use of low herbicides doses for yield improvement economically too risky for most farmers.

Recent research that removes part of the environmental variation may provide the breakthrough needed to exploit herbicide hormesis for crop production. Krenchinski et al. (2024a; 2024b), provide a new approach of using hormesis to generate more consistent, enhanced yields from low glyphosate exposure in glyphosate-resistant (GR) soybeans. Instead of using only a foliar treatment, these studies found that treatment of the soybean seed with low glyphosate doses before planting produced more consistent and greater increases in growth and yield production than only foliar applications. They found increases (11 to 42%) in soybean yield with 90 g ae ha^-1 glyphosate applied to seeds alone or applied to seeds plus an additional 90 g ae ha^-1 glyphosate foliar spray at the V3 stage with four GR cultivars tested at four different field locations (Krenchinski et al., 2024b) (Figure 2). In comparison, the foliar treatment alone was much less effective in eliciting a hormetic effect on yield. The seed treatment alone was reasoned to work better than a foliar treatment alone at least partly because of the higher uniformity of dose reaching each seed/plant. With foliar applications, there is always a range of doses reaching sprayed individual plants, only some of which elicit a hormetic effect, providing the environmental variables allow it. The same effective treatments in increasing yield also increased the number and dry weight of nodules. This new seed treatment approach to reducing the impact of environmental variables and to increasing the uniformity of individual herbicide dose may be a major step needed for utilizing herbicide hormesis more reliably to increase crop yield. For this to be successful, the herbicide used for weed control might need to be different from the one used as a hormetic growth regulator. In the Krenchinski et al. (2024b) study, glyphosate was used for weed control, but the crop was shielded from this application.

Figure 2
Crop yield of soybean RR2 (M5917-IPRO and M5838-IPRO) and RR (BMX-Tornado and N5909) cultivars treated with glyphosate via foliar (90 g ae ha−1), seed (90 g ae ha−1), and seed + foliar (180 g ae ha−1) in Assis Chateaubriand, Botucatu, Marechal Cândido Rondon, and Palotina, Brazil. Mean ± confidence interval (5% probability). Same capital letters between locations, italic capital letters between cultivars, and lowercase letters between treatments within a cultivar did not differ from each other using the Tukey test (p ≤ 0.05). ns—not significant. From Krenchinski et al. (2024b) with permission

Innovative approaches such as that of Krenchinski et al. (2024b) may eventually lead to some herbicides being used at ultralow doses to improve crop yields. Considering the complexity of environmental factors and biochemical and physiological factors that interact to cause hormesis, Rico-Chávez et al. (2022) have proposed that artificial intelligence approaches (e.g., machine learning and deep learning) be used to better utilize hormesis for crop improvement.

3.Hormesis effects on weed management and herbicide resistance

Even with the best application technology, a range of doses of herbicide will reach the weeds within and near a sprayed field due to many factors (Velini et al., 2017). Some weeds will be exposed to a hormetic herbicide dose (e.g., Olszyk et al., 2024). Does hormesis influence resistance or other responses to herbicides by weeds?

Herbicides can: (1) cause changes in the abundance of different weed species or individuals of the same species with variable susceptibility in a field without selecting for resistance and can (2) select for evolution and spread of herbicide resistance in a weed species. Hormesis can contribute to both of these processes in different ways and both processes are likely to occur inseparably side by side and to affect each other.

In the first case, a herbicide dose that has little effect on the growth of weed species A, while killing or greatly reducing growth of weed species B will eventually cause the presence of species A to increase without evolution of resistance. If the effect of that dose on species A is hormetic, the species shift should be even faster, as a more robust plant should be more likely to contribute to the next generation of that species. In a laboratory study, Belz et al. (2011) found the natural phytotoxin parthenin to be stimulatory (32% on average) to growth of Lactuca sativa L. at a concentration that reduced growth of two weed species (Ageratum conyzoides L. and Glysophila paniculate L.) by about 80%. Similar situations between two weed species are certain to occur with some herbicides in field situations, thereby affecting weed management without evolution of resistance. For example, use of a single herbicide that does not kill certain species or vigorous individuals of the same species will result in species shifts to the tolerant (not evolved resistance) species or subpopulation (e.g., DiTomaso, 2017; Grundy et al., 2011). The apparent evolution of enhanced herbicide hormesis without evolution of resistance after years of exposure to a herbicide (Ethridge et al., 2023) that is discussed in detail below may contribute to such a phenomenon.

Hormesis may also contribute to the problem of herbicide resistance. The evolution and spread of herbicide resistance have become major problems in crop production (Heap, 2014; 2024). Recurrent exposure of weeds to sublethal doses of herbicides is known to select for herbicide resistance, especially non-target site resistance (NTSR) (e.g., Busi, Powles, 2009; Gaines et al., 2020; Rigon et al., 2023). Does exposure to hormetic (subtoxic) herbicide doses also contribute to evolution of herbicide-resistant weeds? There is growing evidence that herbicide hormesis plays a role in changes in weed population sensitivity to herbicides (Belz et al., 2022), as insecticide and fungicide hormesis have been proposed to contribute to evolution of insecticide and fungicide resistance (Gong et al., 2022; Agathokleous, Calabrese, 2021, respectively). Hormesis is becoming recognized as an important contributor to evolutionary responses to toxicants in general (Sebastiano et al., 2022).

If hormesis contributes to evolution of herbicide resistance, whether the resistance is target-site resistance (TSR) or NTSR is likely to influence its role. NTSR generally provides a lower level of resistance than TSR (Gaines et al., 2020). NTSR is also more likely to be multigenic than TSR, especially over time, as various genes that each provide a limited level of resistance accumulate and combine in NTSR biotypes, causing the level of evolved resistance to increase over time. This selection for gradual accumulation of resistance genes is termed ‘creeping’ resistance by Gressel (2009). Alleles of genes providing NTSR are more likely to be present or present to a greater level in existing weed subpopulations than those that provide TSR, depending on the molecular target. Under field conditions in which recommended herbicide doses are applied, hormetic doses may be more common for TSR than NTSR weeds. Half the recommended dose of tribenuron-methyl, a dose that would be common in sprayed fields, was hormetic to biotypes of Centauria cyanus L. that had already evolved TSR to this herbicide (Stankiewicz-Kosyl et al., 2024). In cases such as this, hormesis could promote the spread of existing resistant TSR biotypes.

Belz et al. (2022) provide evidence that in herbicide-susceptible populations of weeds, hormesis gives more vigorous subpopulations an advantage, regardless of whether the individuals are resistant or just less susceptible. For example, hormetic increases in barley spike length with glyphosate was only found with the fastest growing subpopulation (>95^th percentile) (Belz, Sinkkonen, 2021). This subpopulation was also less susceptible to glyphosate than the slowest growing subpopulation (<5%). The faster growing subpopulation was found to have a 2.7-more tolerant response to glyphosate than the population as a whole (Belz, Sinkkonen, 2019; 2021). Thus, herbicide hormesis should promote the survival and propagation of a more tolerant/resistant subpopulation, leading to evolution of resistance. With a crop like barley, one might assume that the genetic variation with regard to glyphosate tolerance would be relatively low, but the hormetically enhanced, faster-growing population produced more and bigger seeds and plants that were more tolerant than the untreated general population (Belz, Sinkkonen, 2021). In weed populations with much more genetic variation, including more NTSR alleles of genes, such an effect might provide a greater contribution to the evolution of resistance.

Evolutionary advantages can be due to more vigorous growth that provides a competitive advantage and/or increased seed production and seed vigor. Herbicide hormesis can increase both parameters, giving weed species subpopulations that exhibit pronounced hormesis an evolutionary advantage when subjected to a hormetic herbicide dose. This is obvious in cases of pronounced hormetic increase in plant size and vigor, as seen in Figure 3. In this same example of glyphosate hormesis in a glyphosate-susceptible biotype (Figure 3A), seed number was also increased with a low glyphosate dose (Mobli et al., 2020). In the example of Conyza sumatrensis (Retz.) E. Walker in Figure 3B, a paraquat-resistant biotype produced 60% more seed buds per plant at the paraquat concentration that stimulated growth the most (125 g ae ha^-1) (Asaduzzaman et al., 2022).

Figure 3
A. Glyphosate hormesis in the weed Sonchus oleraceus L. 42 days after application of the herbicide. Reproduced from Mobli et al. (2020) with permission. B. Paraquat hormesis in a resistant biotype of Conyza sumatrensis (Retz.) E. Walker. Reproduced from Asaduzzaman et al. (2022) with permission

Year after year of exposure of weeds to low herbicide doses might favor subpopulations with more robust hormetic responses. Ethridge et al. (2023) reported that glyphosate can select for enhanced herbicide hormesis. Seeds of Abutilon theophrasti Medik. were collected in 1988, 1995, 2002, 2009, and 2016 from a field routinely treated with glyphosate during this 28-year time span and stored in a seed bank vault. Then, seed from each collection were increased in the greenhouse in 2018 in a manner that prevented cross pollination. They found the hormetic response (total plant dry weight) to glyphosate increased from no hormesis with the seeds from the 1988 accession, low hormesis with 1995 and 2002 accession seeds, and robust hormesis with the 2009 and 2016 accession seeds (Figure 4). However, no glyphosate resistance evolved, as the dose that inhibited growth by 50% was the same in plants from seeds from all accessions. These results indicate that subpopulations with a strong hormetic response to glyphosate have a survival advantage.

Figure 4
Plant dry weight of Abutilon theophrasti Medik. of five year-lines in response to increasing doses of glyphosate. The lines are the best fit Brain–Cousens model. The P value indicates the significance of the increase in plant dry weight in the hormesis region of the curve in comparison to the nontreated control based on a one-tail t-test. Redrawn from Ethridge et al. (2023).

Recommended application doses that are hormetic to herbicide-resistant weeds can enhance their propagation and spread (Belz et al., 2022). For example, a recommended field dose of fenoxaprop-P-ethyl kills the sensitive biotype of Alopoecurus myosuroides Huds., while stimulating growth of a resistant biotype (Petersen et al., 2008) (Figure 5). The same resistant biotype was also stimulated by a dose of cycloxydim just below the recommended field dose, a dose that one might expect some of the weed population to receive. Likewise, a dose of metamitron just below the field dose that kills susceptible Chenopodium album L. stimulates the growth of a resistant biotype (Belz et al., 2011). A recommend field application dose of glyphosate caused hormesis in a GR biotype of Erigeron bonariensis L. (Granados et al., 2023). Thus, herbicide hormesis can contribute to the success and spread of existing herbicide-resistant weed biotypes.

Figure 5
Differential susceptibility of sensitive and resistant biotypes of Alopecurus myosuroides Huds. to fenoxaprop-P-ethyl (FEN) (A) or cycloxydim (B) and of Chenopodium album to metamitron (C) after spray application in greenhouse studies. Grey bars represent recommended herbicide doses. Biotype RotHa with ACCase target-site mutation had a maximum stimulation of 39% at increased FEN doses and a maximum stimulation of 54% at reduced cycloxydim doses. Biotype 635 with ACCase target-site mutation had a 25% increase with reduced cycloxydim doses. Biotype 177 with suspected triazinone resistance showed a maximum stimulation of 104% at reduced metamitron doses (redrawn from Belz et al., 2011).

As pointed out by Belz et al. (2011), growth enhancement may not directly influence the spread of a resistant biotype unless accompanied by enhanced reproductive success. Coupling reproductive success with greater growth in a field situation is likely for three reasons. First, some reproduction of many weed species is through asexual propagation by production and growth of propagules (e.g., tubers and rhizomes). Hormesis from foliar applications of herbicides is generally manifested in enhanced root growth, often greater than enhanced shoot growth. Second, enhanced growth and greater biomass generally provides a competitive advantage, and better competitors generally produce more offspring by either sexual or asexual reproduction. Lastly, both growth and reproductive metrics (e.g., flowering, seed production seed weight, seed vigor) have both been enhanced in numerous herbicide dose-response studies producing hormesis in the absence of competition (e.g., Anunciato et al., 2022; Cesco et al., 2024; Mobli et al., 2020). These effects can occur with both herbicide-susceptible and -resistant biotypes at some herbicide dose, but are more likely in the field at recommended herbicide doses with resistant biotypes.

Herbicide hormesis can help select for alleles that contribute to herbicide resistance, whether TSR or NTSR. Once resistance is present, herbicide hormesis in herbicide-resistant biotypes is likely to speed their propagation and spread if the herbicide to which they are resistant is still used for control of other species.

4.Understanding the mechanism(s) of herbicide hormesis

Hormesis has been found with almost all stressors (Erofeeva, 2022), including almost all herbicides with a range of molecular targets (Belz, Duke 2014; 2017; Jalal et al., 2021). Thus, herbicide hormesis is apparently not exclusively associated with any particular mode of action or herbicide molecular target, but is due to secondary effects of any subtoxic level of stress, no matter what the cause of the stress. Glufosinate may be an exception, as low doses can stimulate the activity of its target enzyme glutamine synthetase, and this in vitro effect correlates with in vivo hormesis (Dragićević et al., 2013). It is generally accepted that hormesis is caused by an adaptive response to mild stress that is manifested in the form of overcompensation (Erofeeva, 2022). However, the biochemical and physiological mechanism(s) of herbicide hormesis is/are still not well understood.

Hormesis appears to be more common, reproduceable, and more pronounced with glyphosate than with other herbicides (Cedergreen et al., 2007; Brito et al., 2018). The only study of which we are aware that compared hormesis between herbicides with different mode(s) of action/target sites (acifluorfen/protoporphyrinogen oxidase; diquat/photosystem I; haloxyfop/acetyl CoA carboxylase; MCPA/auxin mimic; metsulfuron/acetolactate synthase; pendimethalin/microtubules; terbuthylazine/photosystem II) with that of glyphosate in the same bioassays was conducted with barley (Hordeum vulgare L.) by root feeding or foliar spraying the herbicides in separate experiments (Cedergreen, 2008). The effects of the herbicides at a wide range of doses on the entire (root plus shoot) dry weight of the plants was determined. Glyphosate hormesis was found with either method of application in both replications of the experiment. This was not the case for the other herbicides, except for the ALS-inhibitor metsulfuron, supporting the view that glyphosate hormesis is more reproduceable than hormesis with most other herbicides. Both glyphosate and metsulfuron are systemic herbicides, which may contribute to more reproducible hormesis.

A large fraction of the papers on herbicide hormesis found in Figure 1 are on glyphosate hormesis. For example, 1,240 of the 2,660 herbicide hormesis papers published between 2011 and 2020 were on glyphosate hormesis. Part of the reason for this may be that glyphosate is the most used herbicide worldwide (Benbrook, 2016; Maggi et al., 2020), making glyphosate hormesis of more interest than hormesis associated with other herbicides. However, the more pronounced and more reproduceable hormesis with glyphosate than with other herbicides probably also plays a role the disproportionate interest in glyphosate hormesis. There may be a factor or factors unique to glyphosate hormesis that adds to or synergizes with the mild stress involved in hormesis caused by other herbicides. The additional factor or factors are likely to be associated with glyphosate’s unique mode of action, inhibition of the enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) (Duke, 2020), an enzyme of the shikimate pathway (Figure 6). The very high glyphosate resistance factors (50 to 100-fold) of transgenic plants with transgenes encoding a GR form of EPSPS (Hetherington et al., 1999; Nandula et al., 2007) provide strong evidence that glyphosate has no other molecular target, even at very high application doses. Thus, the generally higher reproducibility, occurrence, and magnitude of hormesis with glyphosate compared to other herbicides is probably associated with its inhibitory mode of action, rather than to a secondary molecular target.

Figure 6
The shikimate pathway and effects of inhibition of EPSPS by glyphosate (green arrows indicate increases and grey arrows indicate decreases)

The shikimate pathway (Figure 6) provides plants with aromatic amino acids (phenylalanine, tyrosine, and tryptophan) that are needed for protein synthesis. The shikimate pathway intermediate chorismate is a precursor for ubiquinone (UQ), phylloquinone, and folate. UQ is required for mitochondrial election transport and is a cofactor of dihydroorotate dehydrogenase (DHODH), an enzyme required for pyrimidine biosynthesis and the novel molecular target of a herbicide (tetflupyrolimet) that will soon be commercialized (Kang et al., 2023). UQ is a requirement in various other enzymatic processes and is highly involved in antioxidant functions in plant cells (Liu, Lu, 2016). Phylloquinone is a required electron transport component of photosystem I (Srinivasan, Golbeck, 2009). Folate is an essential cofactor for several enzymes. The three aromatic amino acids are precursors for other compounds that are essential for plant growth and development. For example, tyrosine is a precursor of plastoquinone (PQ). PQ is required for photosystem II electron transport and is a cofactor for phytoene desaturase, a key enzyme in carotenoid biosynthesis. Both functions are needed for a functional chloroplast. Tyrosine is also a precursor of tocopherols needed as antioxidants in plants. Tryptophan is a precursor of indoleacetic acid (IAA), a hormone needed for plant growth and development. Loss of any one of these shikimate pathway products thus far mentioned would be lethal. Even though many of the other shikimate pathway products are termed ‘secondary products’ (e.g., flavonoids) and may not be essential for the plant to survive under laboratory conditions, some of these secondary compounds are needed for the survival of higher plants in a natural environment. For example, lignin (derived from both phenylalanine and tyrosine) is required for higher plant cell, tissue and organ development and responses to both biotic and abiotic stresses (Liu et al., 2018). No other plant biosynthetic pathway produces so many different compounds that are required for plant survival. The large number of essential compounds produced by the shikimate pathway and the large amount of lignin produced in many plant species results in a large amount of carbon moving through this pathway (Bentley, 1990). Thus, inhibition of the shikimate pathway affects almost every aspect of plant growth and development in a more direct manner than inhibition of other herbicide molecular targets.

Another feature of glyphosate is that, once taken up, it is readily translated throughout the plant, especially to metabolic sinks such as meristems (Duke, 2020). Subtle effects of systemic herbicides such as glyphosate may be more reproducible than those of contact herbicides that are less evenly distributed in plant tissues.

How does a hormetic dose of glyphosate affect some of these essential physiological functions in a way that would promote hormesis? To do so, at least some EPSPS must be inhibited. Unlike glufosinate (Dragićević et al., 2013), there is no evidence that low glyphosate concentrations increase activity of its target. Little is known about how much of a herbicide molecular target must be inhibited to cause phytotoxicity (Dayan, Duke 2020). Inhibition of EPSPS by glyphosate results in increases in activity of the first enzyme of the pathway, 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (DAHPS), through loss of feedback inhibition (Pinto et al. 1988). Thus, inhibition of EPSPS should cause more carbon to enter the shikimate pathway, due to elevated DAHPS activity. No study has measured carbon flow into the shikimate pathway before and after inhibition of EPSPS. However, loss of feedback inhibition probably contributes to elevated shikimate, quinate, and benzoate levels in response to glyphosate treatment. EPSPS is unique as a herbicide target, in that there is a highly sensitive biomarker for its in vivo inhibition. The large and rapid increases in shikimate in glyphosate-treated plants provide a robust biomarker for in planta inhibition of the enzyme. This effect has been used by many researchers to determine exposure of plants to glyphosate (e.g., Singh, Shaner, 1998; Shaner et al., 2005; Duke, 2020). Thus, increases in shikimate levels in plants treated with glyphosate indicate that at least some EPSPS in some of the cells of the sampled tissues is inhibited.

Few studies of hormetic doses of glyphosate have measured effects on shikimate levels, and when they have been measured, the results have been inconsistent. For example, in a study with glyphosate-susceptible soybean, hormetic glyphosate doses had no effects on shikimate levels at 7 days after application, but a second hormetic glyphosate dose to the same plants increased shikimate levels (Silva et al., 2016). There were small increases in shikimate in lettuce roots at glyphosate doses that caused increased root growth in one experiment, but effects could not be reliably induced in identical experiments (Belz, Leberle, 2012). Both shikimate and quinate were increased in sugarcane with a hormetic glyphosate dose (1.8 g ha^-1) (Pincelli-Souza et al., 2020). Relatively large increases in shikimate in glyphosate-susceptible soybean and maize at hormetic doses were found (Velini et al., 2008).

At hormetic doses of glyphosate, one can assume that only a small fraction of EPSPS is inhibited and that the fraction of EPSPS affected is much smaller in some cells than others. Glyphosate is preferentially translocated to developing cells (Duke, 2020) which represent a small proportion of the plant tissues that are extracted for assay of metabolites such as shikimate. Thus, the small and sporadic effects of hormetic doses of glyphosate on shikimate and shikimate derivatives reported are expected to be proportionally much smaller than the effects in developing tissues – effects that are diluted by extracting whole plant organs (e.g., roots or leaves). Thus, the hormetic effects on growth are probably mostly or entirely due glyphosate’s effects on developing cells that have a significant, but difficult to measure, percentage of their EPSPS inhibited.

Little is known about how carbon is allocated to the different products of the shikimate pathway. Deposition of lignin in the cell walls of developing plant cells, increases rigidity and eventually stops cell expansion. Thus, delayed and/or reduced deposition of lignin would allow for extended cellular expansion, leading to enhanced longitudinal plant growth. This theory has been previously proposed (Duke et al., 2006; Velini et al., 2008). Because such a relatively large amount of carbon flows into the shikimate pathway, its blockage may also result in more carbon available for other pathways, even though deregulation of the shikimate pathway (Pinto et al., 1988) may partly compensate for this.

If the proposed role of lignin in glyphosate hormesis is correct, one might expect glyphosate hormesis to be more pronounced and more easily detected in woody plants with high carbon flow into lignin. There are studies of hormetic effects on woody plants that produce 100% or more increases in plant height by low glyphosate doses (e.g., de Faria et al., 2023). We report the % total plant weight as affected by low glyphosate doses in herbaceous and woody plants in Table 1. We only considered effects on total plant weight, as examining only shoot, root, or plant organ (e.g., stem or leaf) effects might mask effects on carbon distribution, concealing no increase or even a decrease in total plant biomass. For example, Brain et al. (2005) found a tetracycline mixture to increase plant height of Myriophyllum spicatum L., while decreasing root length and dry weight of the entire plant. Relatively few hormesis studies provide effects on total plant weight. Averaged over all species of Table 1, levels of percent increase in growth with low glyphosate doses are, however, similar in woody (33 %) and herbaceous (37%) species (Table 1). However, we know that conditions for whether and what level of hormesis occurs vary between species, and it is unlikely that optimal conditions were present in all of the cases listed in Table 1. This analysis is inconclusive, but if there was a dramatic enhancement of glyphosate hormesis in woody versus herbaceous plant species, we expect it would have been seen in this analysis.

Table 1
Levels of glyphosate hormesis in herbaceous vs. woody plant species.

Plant species	% growth stimulation/g ae ha-1 glyphosate1	Reference
herbaceous
Carthamus tinctoris	31/45	Dos Santos et al., 2021
Commelina benghalensis	43/0.2	Velini et al., 2008
Coronopus didymus	6/32	Nadeem et al., 2016
Chenopodium album	41/16-42	Nadeem et al., 2016
Digitaria insularis	50/15	Anunciato et al., 2022
Echinocloa crus-galli	20/?	Schabenberger et al.,1999
Hordeum vulgare	33/33	Cedergreen, 2008
Lathryus aphaca	37/8	Nadeem et al., 2016
Rumex dentatus	81/16	Nadeem et al., 2016
Sonchus oleraceus	40-180/5	Mobli et al., 2020
Urochloa decumbens	20-30/11	Moraes et al., 2020
Zea mays	20/?	Wagner et al., 2003
woody
Coffea arabica	27/513	Carvalho et al., 2013
Coffea arabica	15/17	Costa et al., 2023
Eucalyptus grandis	70/3.7	Velini et al., 2008
Pinus caribaea	21/5.4	Velini et al., 2008

• ¹ Values are percent growth stimulation, followed by the glyphosate dose used.

Glyphosate hormesis has been found to occur with unicellular microalgae, including cyanobacteria (Dabney, Patiño, 2018; Chávez-Montez, 2024; Qiu et al., 2013; Solomonova et al., 2024a; 2024b; Zhang et al., 2016). Unicellular algae produce no lignin (Martone et al., 2009). In some of these cases (Qiu et al., 2013; Solomonova et al., 2024a; 2024b), growth enhancement by glyphosate was attributed at least in part to the use of glyphosate by the P-starved alga as a source of phosphorus. Glyphosate as a nutrient source as an explanation of glyphosate stimulation cannot be involved for the cases of glyphosate hormesis reported in higher plants, as they have not been P-starved in these studies, and they would have to metabolize glyphosate with a C-P lyase, an enzyme that has not been found in higher plants, even though there are a few reports of glyphosate degrading to sarcosine (a C-P lyase product of glyphosate) in some plant species (Duke, 2025). Furthermore, the level of growth stimulation of the P-starved microalga Isochrysis galbana Parke was increased four-fold by glyphosate (Solomonova et al., 2024a), a hormesis level not seen in terrestrial plants. In the case of glyphosate hormesis of the dinoflagellate Prorocentrum cordatum, is was speculated that bacteria in the cultures contributed to the break down of glyphosate to provide P for the alga (Solomonova et al., 2024b). Cedergreen et al. (2016) found glyphosate hormesis in P-starved duckweed, but not in P-starved barley. They hypothesized that glyphosate hormesis in P-starved duckweed is due to utilization of glyphosate as a P source, although they did not rule out contamination of their glyphosate with phosphate. If there was no phosphate in their glyphosate, was a plant or a microbial C-P lyase involved in breaking down glyphosate, and does this process occur in other P-deficient plant species? Dabney and Patiño (2018) found that glyphosate-caused hormesis with the alga Prymnesium parvum occurred in P-sufficient media and concluded that the hormesis could not be due to the relatively small amount of P that might be produced degradation of glyphosate. We have found only one report of glyphosate hormesis with a bacterium - a low dose of glyphosate promoted growth of Photobacterium phosphoreum by 26% (Si et al., 2024). Considering the results of Table 1 and the level of glyphosate hormesis of algal species without lignin (with other sources of P available), our previous hypothesis that there are preferential effects on lignin synthesis when the shikimate pathway is only slightly inhibited may be wrong or only one of several processes involved in glyphosate hormesis.

Indications of low levels of oxidative stress, including activation of antioxidant defenses, are often found in conjunction with hormesis in both plants and animals, regardless of the stressor (e.g., Nitti et al., 2022; Zhang et al., 2020), including glyphosate (e.g., Bortolheiro et al., 2023; Santos et al., 2022). A recent paper even accredits activation of just one gene (Nrf2) encoding a transcription factor that mediates anti-oxidant and anti-inflammatory adaptive responses as being the principle hormetic mechanism (Calabrese, Kozumbo, 2021). Although neither this gene nor any homologs of it are found in plants (Gacesa et al., 2015), other genes involved in responses to oxidative stress could be involved in herbicide hormesis in plants. Stress in general results in production of reactive oxygen species (ROS) (Choudhury et al., 2017). Thus, subtoxic concentrations of herbicides that result in hormesis are most probably causing sufficient stress to result in ROS production. Herbicides that directly inhibit photosystems II (e.g., diuron), divert electrons from photosystem I (e.g., paraquat), or cause the accumulation of a photodynamic compound such as protoporphyrinogen oxidase inhibitors (e.g., lactofen) generate ROS as an integral part of their modes of action, whereas herbicides with other modes of action generate ROS as a secondary effect of stress (Traxler et al., 2023).Yet, hormesis appears to be no more pronounced with herbicides that more directly produce ROS than others. For example, using the same bioassay, Cedergreen (2008) found no greater hormesis with herbicides that cause ROS as an integral part of their modes of action (diquat, terbuthylazine, and acifluorfen) than with those in which ROS does not pay an integral role in their modes of action (glyphosate, haloxyfop, MCPA, metsulfuron, and pendimethylin). The reduction of several shikimic acid pathway products (Figure 6), such as UQ, phylloquinone and PQ would result in ROS production from blocked electron transport. This would be particularly true for phylloquinone and PQ, which function in the chloroplast, where the molecular oxygen levels are high in light. Indeed, indications of ROS production by hormetic doses of glyphosate have been reported (e.g., Bortolheiro et al., 2023; dos Santos et al., 2022; Wang et al., 2024). The induction of antioxidant enzymes, superoxide dismutase, catalase, and peroxidase by a hormetic glyphosate treatment of tomato was associated with protection from diuron (Wang et al., 2024).

Biomass could not be increased without increased carbon fixation, which requires a direct or secondary enhancement of photosynthesis by herbicide hormesis. Many studies of herbicide hormesis have reported enhanced photosynthetic parameters, including chloroplast pigment content, electron transport rate, stomatal conductance, etc. (e.g., Silva et al., 2016; Nascentes et al., 2018; Cedergreen, Olesen, 2010; Carvalho et al., 2012). These parameters are enhanced with herbicide hormesis, regardless of the herbicide mode of action and are associated with hormetic effects of other stressors on green plants as well (Agathokleous, 2021). Thus, a direct effect on photosynthesis of the stressor is apparently not required for induction of hormesis. Erofeeva (2024) has reviewed the role of net energy surpluses (greater carbon assimilation than respiration) in plant hormesis.

Understanding what genes are up- or down-regulated by hormesis could be useful in engineering crops with higher productivity. Thus, transcriptomics might provide a clue as to what genes and thereby which biochemical and physiological processes are directly involved in herbicide hormesis. As with metabolites, transcriptome study results are most always from homogenization of several cell types with different exposures to a toxicant (e.g., Díaz-Tielas et al., 2019), which probably masks any dramatic effect(s) in a particular cell type. An experiment with a plant with only one cell type that is uniformly exposed to the same glyphosate dose may provide a clearer view of what genes are most likely involved in glyphosate hormesis.

Chávez-Montez et al. (2024) examined effects of a hormetic dose of glyphosate on the unicellular alga Prymnesium parvum N. Carter at 9 days after exposure. There were ten times more genes up-regulated than down-regulated by glyphosate at a dose causing growth stimulation. The upregulated genes were primarily associated with metabolism and biosynthesis; however, EPSPS transcripts were not affected at the hormetic dose. The hormesis was accompanied by upregulation of genes associated with photosynthesis and chloroplast pigment synthesis. The authors concluded that the hormesis was a consequence of a general increase in metabolic and biosynthetic activities driven by a predominantly upregulated transcriptome. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis of the affected genes in different metabolic pathways provided no insight into the mechanism of hormesis, other than upregulation of some genes associated with stress and antioxidant activity. Because these plant cells were immersed in the glyphosate solution, it is likely that the herbicide was taken up rapidly and uniformly by the entire cell population. Thus, the primary effects probably took place much earlier than 9 days after treatment. After 9 days, mild stress may have been over, due to the overcompensation that is triggered in hormesis.

Two studies have been made on transcriptome effects of hormetic concentrations of cadmium (Cd) on plants (Ma et al., 2022; Wang et al., 2023). In a study on broccoli exposure to a hormetic dose of Cd, transcriptome analysis suggested involvement of hormone signaling and secondary metabolism (Ma et al., 2022), whereas in a study of Cd-induced hormesis in peppermint, transcriptome analysis suggested involvement of phenylpropanoid metabolism and antioxidant activity (Wang et al., 2023). No clear determination of a mechanism of induced hormesis was determined in either study, however, the involvement of elevated antioxidant activity appears to be common to herbicide hormesis studies.

Transcriptomics can provide a detailed assessment of the transcription status of all the genes of an organism as affected by a herbicide; however, trying to find a single mechanism of anything with this method has been problematic (Duke et al., 2013). The transcriptomic response can vary considerably with different herbicide doses and different times after application of the herbicide. We assume that transcriptomic responses of different cell types in different plant organs will vary significantly, especially when they have different exposures to a herbicide applied at a low dose. Also, there can be quite different results with transcriptomics and proteomics. For example, using the same tissues from the same experiment carried out at the same time, the effects of the phytotoxin cantharidin on the transcriptome and proteome of Arabidopsis were quite different (Bajsa et al., 2011; 2015). We assumed that posttranslational modifications of proteins may have played a role in this disparity. The fact that the molecular target of cantharidin in plants is serine/threonine protein phosphatases (Bajsa et al., 2012) could not have been determined from either the transcriptome or proteome data from these papers.

5.Conclusions

The volume of research on hormesis caused by herbicides in crops, weeds, and other plants, including algae, has grown dramatically in the past decade. More successes in using low herbicide doses to improve crop yield have been reported, although we assume that many unsuccessful attempts to use low herbicide doses to improve crop yields go unreported. A notable success is the use of a seed treatment with a low glyphosate dose, followed by a low dose after seedling emergence, to provide more predictable hormesis in the field, resulting in significant and reproduceable increases in crop yield. The potential of herbicide hormesis to contribute to weed management problems is becoming more clearly understood. In rare cases, recommended herbicide doses that may overlap the hormetic dose range of a weed species make that species more problematic. Hormetic herbicide doses for weed subpopulations that are more tolerant/resistant than that for most of the plants in a weed population can accelerate the selection for and spread of herbicide resistance. This phenomenon needs further study and documentation. The molecular mechanism(s) of herbicide hormesis is/are still unknown, although overcompensation for mild stress caused by low herbicide doses appears to common to all herbicide hormesis. Glyphosate hormesis appears to be more consistent and pronounced than that with other herbicides, which might be related to relatively large number of essential compounds produced by the shikimic pathway and to the highly systemic movement of glyphosate in plants. Focusing on the effects on the most affected cells in a plant might clarify the mechanism(s) of herbicide hormesis.

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• Funding:
  This research was funded in part by USDA, ARS, grant/award number: 58-6060-6-015.

Edited by

• Approved by:
  Editor in Chief: Carol Ann Mallory-Smith
  Associate Editor: Aldo Merotto Junior

Publication Dates

• Publication in this collection
  25 Apr 2025
• Date of issue
  2025

History

• Received
  7 Nov 2024
• Accepted
  3 Feb 2025