- Open Access
Loss-of-function in GIGANTEA confers resistance to PPO-inhibiting herbicide tiafenacil through transcriptional activation of antioxidant genes in Arabidopsis
Applied Biological Chemistry volume 65, Article number: 66 (2022)
Herbicides play a crucial role in maintaining crop productivity by reducing competition between weeds and crops. Protoporphyrinogen oxidase (PPO)-inhibiting herbicides trigger the photooxidative damage that destroys cell membranes. Tiafenacil is a recently developed pyrimidinedione-type PPO-inhibiting herbicide that has low IC50 values in plants and is less toxic in humans compared to other PPO inhibitors. Previous reports confirmed that mutations in Arabidopsis circadian clock-controlled gene GIGANTEA (GI) were insensitive to phytooxidants, including chloroplast biogenesis inhibitors and herbicides. Here, we examined whether GI regulates the resistance to tiafenacil. Both gi mutant alleles, gi-1 and gi-2, were resistant to tiafenacil with survival rates of 97% and 83%, respectively, under 1 µM tiafenacil treatments, while 56% of wild-type and GI-overexpressing plants (GI-OX) survived. Both gi mutants were insensitive to tiafenacil-induced inhibition of photosystem efficiency and alleviated photooxidative damage. The gi mutants showed significant increases in transcriptional expressions and enzyme activities of antioxidants compared to wild-type and GI-OX. Moreover, loss-of-function in GI enhanced resistance to tiafenacil-containing commercial herbicide Terrad’or Plus®. Collectively, based on our results together with previous reports, mutations in GI confer resistance to herbicides with different MoAs and would be a crucial molecular target for non-target-site resistance strategies to develop herbicide-resistant crops.
Weed controls are the major activities in agronomics to maintain crop yields and quality as weeds and crops compete for water, nutrients, sunlight, and space availability . Weed controls have been developed from native manual control to modern mechanical, biological, and chemical controls, reducing agricultural labor for crop producers and increasing the effectiveness of controls . Chemical weed control, represented as an herbicide application, is widely used to inhibit the germination or growth of the weed species on cultivated lands .
The Weed Science Society of America (WSSA) and the Herbicide Resistance Action Committee (HRAC) recently classified herbicides into 25 groups based on their herbicide site of action (SoA) (http://wssa.net), which refers to a specific molecular target that the herbicide binds to and its binding disrupts the biological process (referred to a mode of action, MoA) in weed plants resulting in the death . Herbicide MoAs vary like lipid synthesis inhibitors, amino acid synthesis inhibitors, growth regulators, photosynthesis inhibitors, nitrogen metabolism inhibitors, pigment inhibitors, cell membrane disruptors, and seedling growth inhibitors.
The protoporphyrinogen oxidase (PPO) inhibitors termed Group 14 belong to cell membrane disruptors, which are the most widely used herbicides to control weeds resistant to glyphosate and acetolactate synthase (ALS) inhibitors . PPO is a key enzyme in the heme/chlorophyll biosynthetic pathway and catalyzes the oxidation of protoporphyrinogen IX to protoporphyrin IX [6, 7]. PPO inhibitors lead to the accumulation of protoporphyrinogen IX in the cytosol, which allows the active oxidation of protoporphyrin IX by light and oxygen . The photosensitive protoporphyrin IX leads to the production of reactive oxygen species (ROS) causing lipid peroxidation and plant death [9, 10]. PPO inhibitors are also sub-classified into diphenyl ethers, N-phenylphalimides, oxadiazoles, oxazolidinediones, phenylpyrazoles, pyridinediones, thiadiazoles, triazinones, and triazolinones .
GIGANTEA (GI) is a highly conserved vascular plant-specific gene displaying pleiotropic phenotypes including flowering time control, circadian period, light signaling, carbohydrate metabolism, abiotic stress responses, and other physiological processes [11,12,13,14,15]. One gi mutant allele, gi-3, showed resistance to oxidative agents, paraquat and hydrogen peroxide . Recently, we reported that other gi mutant alleles, gi-1 and gi-2, were tolerant to herbicide butafenacil, a pyrimidinedione chemical class PPO inhibitor . These results suggest that mutation in GI would display cross-reactivity to various herbicides having different MoAs.
Recently, tiafenacil (Terrad’or Plus®) is developed as a new pyrimidinedione-type herbicide by FarmHannong Co., Ltd., Korea, and registered in the Rural Development Administration of Korea . Tiafenacil is a low toxicity herbicide including low skin sensitization, genotoxicity, and favorable environmental safety, suggesting that tiafenacil is less toxic to growers and a highly effective herbicide to control the annual and perennial weeds .
Here, we investigated whether loss-of-function in Arabidopsis GI enhances resistance to herbicide tiafenacil. To conclude GI involves in herbicide tiafenacil resistance, we carried out phenotypic, molecular, and biochemical analyses using two gi mutant alleles, gi-1 and gi-2, and GI-overexpressing (GI-OX) plants, and the results showed that GI negatively regulates resistance to herbicide tiafenacil with reduced oxidative damage via enhanced antioxidant systems. Furthermore, we also identified that gi mutants are resistant to tiafenacil-containing product, Terrad’or Plus®. Thus, genetic modification of GI would be a powerful non-target-site resistance strategy for developing herbicide-resistant crops.
Mutations in GI confers resistance to herbicide tiafenacil
Paraquat is a fast-acting pyridinium-type herbicide having MoA as a photosynthesis inhibitor that causes oxidative stress in plants . Interestingly, it has been reported that gi mutants (Ler ecotype background, gi-3 to gi-6) were resistant to paraquat and two gi mutants (Col-0 ecotype background, gi-1 and gi-2) were resistant to butafenacil [16, 17, 20]. It raises the possibility that loss-of-function in Arabidopsis GI may confer resistance to various herbicides having different SoAs and MoAs. Thus, we examined whether gi mutants show resistance to the recently developed herbicide tiafenacil using two gi mutant alleles, gi-1 and gi-2, and GI-OX plants. Twenty-day-old plants grown in soils were air-sprayed onto the leaves using different concentrations of tiafenacil. Five days after tiafenacil treatments, the growth of Col-0 (wild-type) plants was gradually inhibited with increasing tiafenacil concentrations (Fig. 1A). By contrast, both gi mutant alleles, gi-1 and gi-2, were less sensitive to tiafenacil treatments compared to Col-0, whereas the tiafenacil-induced injury symptoms of GI-OX plants were sensitive similar to Col-0 (Fig. 1A). Under 1 µM tiafenacil treatments, the survival rate of gi-1 and gi-2 was 96.875% and 82.813%, respectively, and that of Col-0 and GI-OX plants was 56.25% (Fig. 1B). However, the application of 5 µM tiafenacil in all plants resulted in death. The chlorophyll contents in gi-1 and gi-2 were significantly higher than Col-0 under all doses of tiafenacil, and those in GI-OX plants were significantly lower (Fig. 1C). These data suggest that GI negatively regulates herbicide tiafenacil resistance.
gi mutants were insensitive to tiafenacil-induced photosynthetic injury
The PPO inhibitor herbicides result in ROS accumulation in the presence of light disrupting cell membranes, and tiafenacil facilitates injury symptoms light-dependently [5, 18]. PPO inhibitors result in proto accumulation in plants exposed to light, and decrease photosynthetic activity . Thus, we confirmed the Fv/Fm values in gi mutant alleles and GI-OX plants under light or dark conditions. Twenty-day-old plants grown in soils were air-sprayed with water (0 µM tiafenacil) or 100 µM tiafenacil and incubated 18 h in the dark with following 6 h in the light. The Fv/Fm values in all plants slightly decreased after a dark period for 18 h either in the absence or presence of tiafenacil (Fig. 2). The values in Col-0 and GI-OX plants exposed to tiafenacil were rapidly decreased during the subsequent light condition for 6 h, but those in both gi mutant alleles were not changed (Fig. 2B). It suggests that gi mutants did not show the tiafenacil-induced injury in photosynthesis efficiency.
GI negatively regulates tiafenacil-induced oxidative stress
The PPO-inhibiting herbicides including tiafenacil cause injury symptoms, such as necrotic spots and desiccation, on leaves via the herbicide-induced oxidative damage [3, 5, 18]. Thus, we analyzed leaf phenotypes of two-week-old plants three days after 0 or 0.5 µM tiafenacil treatments. Tiafenacil-treated Col-0 and GI-OX clearly showed necrotic spots on the leaves, whereas both gi mutant alleles exhibited minor leaf symptoms (Fig. 3A). Malondialdehyde (MDA) contents in both gi mutants were significantly lower than Col-0 and GI-OX plants (Fig. 3B), suggesting that mutations in GI reduce the tiafenacil-induced oxidative damage in Arabidopsis. Next, we analyzed endogenous ROS levels through histochemical staining and H2O2 contents. DAB staining showed that H2O2 accumulations presented as brown-color precipitates were visible in tiafenacil-treated leaves of Col-0 and GI-OX plants, whereas those in both gi mutant alleles were less than Col-0 and GI-OX (Fig. 3C). We analyzed H2O2 quantification as more direct evidence for endogenous H2O2 levels in plants and data showed that tiafenacil-induced H2O2 accumulation in both gi mutants was significantly lower than that in Col-0 and GI-OX plants (Fig. 3D). These data suggest that loss-of-function in Arabidopsis GI alleviates the herbicide tiafenacil-induced oxidative damage with less accumulation of ROS.
gi mutants exhibit enhanced antioxidant enzyme activity
Oxidative damage by increased ROS levels in plant cells hurts biomolecules and cellular machineries, such as proteins, DNA, lipids, and various cellular compartments [21, 22]. To defend against this oxidative stress, efficient antioxidant systems are necessary to maintain ROS homeostasis via the ROS detoxifying mechanisms including superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), and peroxiredoxin (PrxR) . Thus, we examined whether enhanced tiafenacil resistance in gi mutant alleles is due to the elevated scavenging activity of antioxidant enzymes. The peroxidase (Prx) activity was significantly higher in both gi mutants compared to Col-0 and GI-OX plants, while CAT activity was not significantly different (Fig. 4A). This data is a consistent result with gi-3 under paraquat treatments . In addition, transcriptional levels of antioxidant genes including APX, PrxQ, FeSOD3, MnSOD, and CAT1 were significantly upregulated in the tiafenacil-treated both gi mutants compared to Col-0 and GI-OX plants, whereas CAT2 expression was not significantly different (Fig. 4B). These results suggest that the mutations in Arabidopsis GI increase the transcriptional activation of antioxidant genes, subsequently resulting in enhanced ROS scavenging capacity in gi mutants against tiafenacil-induced oxidative injury.
gi mutants displayed resistance to the Terrad’or Plus®
Non-selective herbicide Terrad’or Plus® containing 24% glyphosate and 0.5% tiafenacil as the active ingredient has been commercially developed by FarmHannong. Thus, we tested whether mutations in Arabidopsis GI also confer the resistance to commercial herbicide Terrad’or Plus®. Under 0.01 mg ml−1 Terrad’or Plus® applications to 20-day-old plants, both gi mutant alleles, gi-1 and gi-2, showed resistance with healthy leaves, while Col-0 and GI-OX plants had severely injured symptoms with inhibition of growth and leaf bleaching (Fig. 5A). Total chlorophyll contents again indicated that gi-1 and gi-2 were tolerant to 0.01 mg ml−1 Terrad’or Plus® with significantly higher chlorophyll contents compared to Col-0 and GI-OX plants (Fig. 5B). MDA contents in both gi mutants under Terrad’or Plus® applications were significantly lower than Col-0 and GI-OX plants, whereas those in all water-treated plants were not significantly different (Fig. 5C). These data suggest that loss-of-function in GI enhances the resistance to commercial herbicide Terrad’or Plus® via reducing the herbicide-induced oxidative damage.
Weed control is essential for maintaining and increasing crop productivity . Due to this reason, the global seed companies are developing herbicide-resistant crops and selling them together with herbicides. One of the best-selling non-selective herbicides is glyphosate with MoA as an amino acid synthesis inhibitor, which inhibits the shikimic acid pathway through blockade of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) [25, 26]. Genetically engineered crops having resistance to glyphosate (named Roundup-ready) were developed in soybean, maize, cotton, canola, and sugar beet . Most recently, mutant variants of the EPSPS gene were tolerant to glyphosate and higher grain yield in rice . Compared to these target-site mutations conferring herbicide resistance, non-target-site resistance would impart cross-resistance to different MoA herbicides [4, 29].
GI is involved in various physiological responses, and its mutations display valuable agronomic traits including prolonged vegetative growth and salt stress tolerance in Arabidopsis, cabbage, and poplar [13, 30,31,32,33]. We have previously found that the gi-2 mutant is insensitive to lincomycin causing chloroplast biogenesis defects . Lincomycin activates the retrograde signaling to repress the expression of photosynthesis-associated nuclear genes and functions similar to norflurazon, belonging to MoA group 12 for inhibition of phytoene desaturase . In addition to these, various gi mutant alleles in different Arabidopsis ecotype backgrounds show resistance to herbicide paraquat and butafenacil, which have different MoA as a photosynthesis inhibitor and a cell membrane disrupter, respectively [16, 17, 20]. Thus, it raises the possibility that genetic modification in GI would apply to generate herbicide-resistant crops against a wide range of herbicides having different MoAs, especially herbicides inducing photooxidative damage.
PPO-inhibiting herbicides are widely applied to control the weeds from cultivated lands. Recently developed herbicide as a new pyrimidinedione-type PPO-inhibiting herbicide by FarmHannong Co. (Republic of Korea), tiafenacil (Terrad’or Plus®) is high affinity to binding to PPOs and has a relatively low half-maximal inhibitory concentration (IC50) values (20–28 nM tiafenacil) against the PPOs from amaranth, soybean, Arabidopsis, and rapeseed compared to other PPO inhibitor herbicides, such as butafenacil, saflufenacil, acifluorfen, oxyfluorfen, and fomesafen . Thus, we investigated GI involved in herbicide tiafenacil resistance using two loss-of-function gi mutant alleles and GI-OX plants. Both gi mutants, gi-1 and gi-2, were resistant to tiafenacil treatment up to 1 µM with a significantly higher survival rate compared to wild-type plants, and the chlorophyll contents in GI-OX plants were significantly lower than wild-type (Fig. 1). Tiafenacil showed significantly lower IC50 to amaranth (20 nM) and rapeseed (28 nM) than butafenacil (29 and 40 nM, respectively), suggesting tiafenacil has a greater inhibitory effect on plant growth to butafenacil . Our previous study showed that both gi mutants were resistant to butafenacil at concentrations of up to 5 µM, while wild-type plants were dead . It reflects the high sensitivity of plants to tiafenacil compared to butafenacil, which is consistent with previous report . PPO-inhibiting herbicides including tiafenacil induce photo-oxidative damage to plants via photosynthetic injury in a light-dependent manner [5, 18], however both gi mutants were insensitive to tiafenacil-induced photosynthetic injury (Fig. 2). The injured symptoms are initially presented as necrotic spots on leaves as a consequence of oxidative stress [3, 18]. Our results showed that application of tiafenacil to gi mutants caused minor injured symptoms, while that to wild-type and GI-OX resulted in the formation of necrotic spots (Fig. 3A). MDA and H2O2 contents are indicators of herbicide-induced oxidative damage in plants, and gi-3 mutant was significantly lower MDA and H2O2 contents and higher antioxidant enzyme activities compared to wild-type plants under paraquat treatments [16, 35]. Our results also showed that both gi-1 and gi-2 were less accumulation of MDA and H2O2 contents and higher antioxidant capacity compared to wild-type and GI-OX plants under tiafenacil treatments (Figs. 3B–D and 4), consistent with the previous report on paraquat and butafenacil resistance of gi mutants [16, 17], suggesting that mutations in GI caused inhibition of tiafenacil-induced oxidative damage via the enhanced antioxidant enzyme activities. Furthermore, both gi mutants were resistant to the tiafenacil-containing commercial herbicide Terrad’or Plus® (Fig. 5).
CRISPR/Cas9-mediated genome editing has been extensively developed as a powerful technique to generate targeted mutations in valuable crop genomes . Despite technical advances, useful genetic materials are still largely absent and need to be elucidated. Through the various physiological, biochemical, and molecular functions of GI in plants reported to date, GI displays pleiotropic phenotypes such as flowering time regulation, light signaling, carbohydrate metabolism, chloroplast biogenesis, and abiotic stress responses [14, 17]. Loss-of-function in Arabidopsis GI causes prolonged vegetative stages, elevated starch accumulation, salt stress tolerance, and insensitivity to photooxidative agents, which are important issues in crop breedings [13, 16, 17, 30, 37]. Furthermore, mutations in GI conferred the cross-resistance to herbicides having different MoA [16, 17]. Thus, GI would be a potential molecular target to develop herbicide-resistant crops with other valuable agronomic traits.
In conclusion, tiafenacil is a recently developed pyrimidinedione-type PPO-inhibiting herbicide. Loss-of-function in Arabidopsis GI confers the resistance to tiafenacil and insensitive to tiafenacil-induced photooxidative damage. Both gi mutants, gi-1 and gi-2, showed less ROS accumulation with enhanced antioxidant capacity under tiafenacil treatments compared to wild-type plants. Together with previous reports, our results suggest that mutations in GI mediate the resistance to a wide range of herbicides having different MoAs, and would be a pivotal molecular target for generating herbicide-resistant crops.
Materials and methods
Plant materials and growth conditions
Arabidopsis thaliana wild-type (Columbia-0 ecotype background, Col-0), GI (AT1G22770)-overexpressing plants (35S:GI-HA, GI-OX) and its two mutants (gi-1 and gi-2) were used in this study [30, 38]. Seeds were sterilized with 30% (v/v) bleach-containing 0.02% (v/v) triton X-100 for 5 min. After stratification in the dark at 4 °C for 2 days, seeds were germinated on Murashige and Skoog (MS) medium for 1 week and transferred to soil for another 2 weeks. Plants were grown in a growth chamber (16 h light/8 h dark cycles, 100 μmol photons m−2 s−1 of white cool fluorescent light) at 22–23 °C for 20 days.
Tiafenacil (methyl N-[2-[[2-chloro-5-[3,6-dihydro-3-methyl-2,6-dioxo-4-(trifluoromethyl)-1(2H)-pyrimidinyl]-4-flurophenyl]thiol-1-oxoprophyl]-ß-alaninate; CAS no. 1220411-29-9]  and Terrad'or Plus® [24% (v/v) glyphosate-isopropylamine and 0.5% (v/v) tiafenacil] were kindly supported from FarmHannong Co., Ltd., Korea. Twenty-day-old Arabidopsis plants grown in soil were treated with foliar spraying of tiafenacil or Terrad'or Plus® (0.01 mg ml−1) onto the leaves.
Determination of total chlorophyll and MDA contents
For measuring chlorophyll contents, herbicide-treated shoot parts of plants were soaked in 80% (v/v) acetone at 23 °C for 48 h in the dark. Chlorophyll a and b were measured spectrophotometrically at 663 and 645 nm, respectively . For measuring MDA contents, herbicide-treated shoot parts of plants were homogenized in the reaction buffer containing 0.5% (w/v) thiobarbituric acid and 20% (w/v) trichloric acid followed by centrifugation at 13,000 rpm for 15 min at 4 °C. Resulting supernatants incubated at 85 °C for 20 min and the reaction was terminated by incubating on ice for 5 min. The absorbance was measured spectrophotometrically at 532 and 600 nm. MDA contents were calculated using an extinction coefficient of 155 mM−1 cm−1 as described previously .
Detection of H2O2 by histochemical staining and quantification of H2O2
Hydrogen peroxide (H2O2) accumulation in the tiafenacil-sprayed plant leaves was stained with 3,3′-diaminobenzidine (DAB, 1 mg mL−1, pH 3.8) and then immersed in 80% (v/v) ethanol to remove the chlorophyll completely to visualize dark-brown staining. The H2O2 contents were determined using the Amplex Red Hydrogen Peroxide/Peroxidase Assay Kit (Invitrogen) according to the manufacturer’s instructions .
For measuring photosynthetic efficiency, plants were foliar sprayed with 0 µM (water) and 100 µM tiafenacil and incubated for 18 h in the dark and subsequent 6 h in the light as described previously . Photosynthetic efficiency was analyzed in each leave with a photosynthesis yield analyzer mini-pam (MINI-PAM, Walz, Effeltrich, Germany) by measuring Fv/Fm value, where Fv = Fm ± Fo. Fo is the minimum and Fv is the maximum value of fluorescence. To determine Fo, plants were dark-adapted for 20 min using a leaf-clip holder. The fluorescence yield was measured when an internal artificial light source was exposed.
Antioxidant enzyme assay
Twenty-day-old plant leaves exposed to 0.5 µM tiafenacil were ground and subjected to antioxidant enzyme assays. Prx and CAT activities were measured using an Amplex Red Hydrogen Peroxide/Peroxidase Assay Kit and Amplex Red Catalase Assay Kit (Invitrogen), respectively, according to the manufacturer’s instructions.
RNA extraction and qRT-PCR
Total RNA was isolated from 20-day-old Arabidopsis plants exposed to tiafenacil with Total RNA Kit (Biofact) following the manufacturer’s instructions. First-strand cDNA was synthesized from 3 μg total RNA with a RevertAid First-Strand cDNA Synthesis Kit (Thermo Fisher Scientific). Synthesized cDNA was amplified by real-time quantitative PCR (qPCR) with a TOPreal™ qPCR 2X PreMIX Kit (SYBR Green with low ROX/Enzynomics) using the CFX96 Touch™ Real-Time PCR Detection System (Bio-Rad Laboratories). The housekeeping gene AT5G12240 was used as the normalization control. The primers used in this study are listed in Additional file 1: Table S1.
Availability of data and materials
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The authors thank Dr. Soon-Kee Sung and FarmHannong Co., Ltd., Korea, for the generous gift of tiafenacil and Terrad’or Plus®.
This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government (MSIT-2022R1A5A1031361), Republic of Korea.
The authors declare that they have no competing interests.
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Cha, JY., Shin, GI., Ahn, G. et al. Loss-of-function in GIGANTEA confers resistance to PPO-inhibiting herbicide tiafenacil through transcriptional activation of antioxidant genes in Arabidopsis. Appl Biol Chem 65, 66 (2022). https://doi.org/10.1186/s13765-022-00734-6
- Herbicide resistance
- Protoporphyrinogen oxidase
- Reactive oxygen species