Weedy rice resistance to imidazolinone herbicides and control with glyphosate

Abstract

Background  Weedy rice (Oryza sativa L.) is a serious competitor of rice, causing severe yield losses. It contaminates and reduces the quality of harvested grain.

Objective  (1) evaluate the response of Colombian weedy rice accessions to glyphosate and the mixture of imazamox + imazapyr (F-IMIs) at commercial rates; (2) determine the resistance level of one morphotype of weedy rice putatively resistant to the F-IMIs from the objective (1).

Methods  Ten weedy rice accessions were evaluated for response to F-IMIs (imazamox + imazapyr 49.5 and 22.5 g a.i. ha^-1, respectively) and glyphosate (960 g a.e. ha^-1). One putative ALS-resistant and five genotypically different accessions were subjected to dose-response assay to determine the level of resistance, or sensitivity, to F-IMIs. The doses included 0, 0.5, 1, 2, 4, 8, and 16; and 0, 0.15, 0.25, 0.5, 0.75, 1, and 2 times the commercial rate of F-IMIs for resistant and susceptible, respectively.

Results  The F-IMIs controlled weedy rice tested (> 71%), except one straw-hull-awned accession (< 5%). The GR₅₀ of weedy rice genotypes ranged from 0.26- to 0.32-fold the commercial rate of F-IMIs, therefore the accessions tested, representing distinct genotypes were susceptible. The resistant strawhull-awned morphotype was 47.04-fold resistant to the F-IMIs based on GR₂₅. Glyphosate controlled all morphotypes and genotypes >90%.

Conclusions  Most Colombian weedy rice can be controlled with IMI herbicides recommended for ALS-resistant rice; however, at least one population evolved resistance to IMI herbicides. Glyphosate is effective on weedy rice populations and can be used before planting rice or after rice harvest.

Weedy Rice; Post-Emergence Rice Herbicide; Herbicide Resistance; Conspecific Species; Clearfield^®

1.Introduction

Rice (Oryza sativa. L.) is one of the most important cereals globally, occupying third place in land use and providing 21% of the calories ingested (Wiebe et al., 2021). Recently, the importance of rice has been further highlighted due to an increase in food demand and supply changes due to the COVID-19 pandemic (Urioste Daza et al., 2020). In the last 10 years, 164 million hectares of rice were cultivated globally every year, with an average production of 500 million tons (US Department of Agriculture, 2024). In Colombia, the total rice production was 1.77 million tons in 536,000 ha on average for this same period (US Department of Agriculture, 2024).

Historically, the average potential yield losses in rice due to weeds have been estimated to be 37% worldwide (Oerke, 2006); However, considering the exponential growth of weed resistance cases to herbicides, potential yield losses in rice is believed to be higher, and highly variable, across countries (Heap, 2024). The greatest rice yield losses were reported in West Africa (30%–100%), Korea (40%–100%), India (25%–85%), Egypt (85%–89%), and Europe (55%–60%), whilst the impact in other countries such as Vietnam (10%–45%), USA (10%–32%), Thailand (35%–40%), Siri Lanka (30%–40%), Malaysia (10%–30%) and Australia (10%–30%) were less (Rao et al., 2007) but still substantial. Central America and South America reported an average yield loss of 20% due to weeds (Oerke, 2006).

Worldwide, weedy rice is a complex of species of the Oryza genus (not well defined taxonomically), hybrids, and special ecotypes (Roma-Burgos et al., 2021b). In many countries, including Colombia, weedy rice is a conspecific species to rice cultivars; it has phenotypic plasticity, high competitive ability, high seed shattering, and deep seed dormancy, causing severe economic losses due to reduced yield and deterioration of grain quality (Delouche et al., 2007). Losses of 40% to 60% have been reported with infestations of 5 to 20 weedy rice plants m^-2 respectively in Colombia (Fisher, Ramirez, 1993). In rainfed and irrigated rice production systems, weedy rice (Oryza spp.) is the most important weed, followed by Echinochloa spp., and Cyperus spp., which together are considered the most common and difficult-to-control weeds due, in part, to their tolerance to hypoxia and herbicides (Kraehmer et al., 2016).

Weedy rice management in Colombia has been widely based on pre-plant burndown with glyphosate (Federación Nacional de Arroceros, 2014). A common weedy rice control technique is the “stale seedbed” which consists of moistening the soil to stimulate weedy rice emergence and subsequent application of non-selective herbicides, generally glyphosate, 30 days before drill seeding. A less popular strategy, is a subsequent application of glyphosate at the spiking stage (S₃) where coleoptiles of weedy rice are visible but not those of cultivated rice (Ziska et al., 2015). This application takes advantage of the rapid emergence and seedling growth of weedy rice, effectively targeting the second cohort of weedy rice emergence, the ones placed at shallow depth after tillage. Some farmers reported suspicions of weedy rice resistance to glyphosate but this matter has not been investigated (Hoyos et al., 2020).

Non-transgenic cultivars resistant to inhibitors of the enzyme acetolactate synthase (ALS) and inhibitors of the acetyl-coenzyme-A (ACCase) herbicides (Clearfield^® [CL] and Provisia^®, respectively) have been commercialized (Ziska et al., 2015). CL rice varieties allow the selective use of herbicides from the imidazolinone family (IMI) and have been widely used in major rice-growing regions globally for more than two decades. Resistance to ALS herbicides among weedy rice populations has been confirmed in regions where CL rice is grown primarily due to gene flow and occasionally as a result of herbicide-selection pressure (Avila et al., 2021a; Roma-Burgos et al., 2021a). The overarching hurdle of weedy rice management is the lack of alternative tools to integrate into systems and the inability of many farmers to practice the technology stewardship guidelines. CL technology was introduced in Colombia between 2003 and 2005; however, it quickly became apparent that crop rotation is constrained by the susceptibility of cotton, corn and sorghum to the residual activity of IMI herbicides following CL (Saldain, 2011). Therefore, CL rice commercialization in Colombia was delayed until 2010 when better practices were adopted.

The diversity of weedy rice (Hoyos et al., 2020; Piveta et al., 2021; Shivrain et al., 2010) underscores the inevitability of resistance evolution to herbicides as such diversity is manifested in differential response to herbicides across populations under various conditions (Avila et al., 2021b; Ferrero et al., 2021; Roma-Burgos et al., 2021a). This context warrants the investigation of representative weedy rice ecotypes and genotypes in Colombia in terms of response to glyphosate and IMI herbicides.

Information about weedy rice in Colombia is scant. This research tested the hypothesis that weedy rice morphotypes and genotypes in Colombia as classified by Hoyos et al. (2019; 2020) differ in tolerance to glyphosate and IMI herbicides. The objectives of this research were to, (I) evaluate the control of ten phenotypically and genotypically distinct Colombian weedy rice accessions to glyphosate and the formulated mixture of imazamox + imazapyr (F-IMIs) herbicides at the commercial rate; (II) to determine the resistance level of one morphotype of weedy rice putatively resistant to the F-IMIs from the objective (I).

2.Material and Methods

2.1 Germination and herbicide application

Weedy rice seed dormancy was broken by incubating the seeds to 50 °C for 12 hours. Petri dishes lined with Whatman^® #1 filter paper and moistened with distilled water (5 ml) were used to germinate the seeds in a growth chamber set at 26–28 °C and 12-hr darkness. Six of these germinated seeds were sown in 120x120x120 mm pots, previously filled with sieved clay soil with 3.9% organic matter and pH 6.5. Pots were placed in the greenhouse at Faculty of Agricultural Sciences, Universidad Nacional de Colombia, Bogotá. The greenhouse environmental condition was 20–34.5 °C and relative humidity between 28.2–65.8%. The herbicide treatments were applied in a spray chamber with a spray boom fitted with one flatfan nozzle (Tee-Jet XR-8001), calibrated to deliver 213 L ha^-1 spray volume at a speed of 0.3 m s^-1 and 1.5 kg cm^-2 air pressure.

2.2 Differential response of weedy rice to the premix of imazamox + imazapyr and glyphosate

From the Colombian weedy rice collection of the Universidad Nacional de Colombia (Hoyos et al., 2020; 2019), five accessions with different hull characteristics (hull color and presence of awn), hereafter called morphotypes, were selected. In addition, five accessions with different ancestry, herein called genotypes, were also evaluated (Table 1). The rice cultivar “Fedearroz-2000” was used as a susceptible control.

Table 1
Description of the selected weedy rice accessions.

Lab ID1	Morphotype description1	Total frequency; and region distribution in Colombia rice production areas2
5C7	Strawhull, awnless, red pericarp (indica-like)	Total: 47%; BJ: 27%, C: 42%, CN: 55%, LL: 55%, S: 64%
5B13	Strawhull, awned, red pericarp (indica-like)
2A2	Brownhull, awned, red pericarp (admixed indica-aus)	Total: 25%; BJ: 33%, C: 25%, CN: 18% ,LL: 18%, S: 27%
2A3	Blackhull, awned, red pericarp (aus-like)	Total: 28%; BJ: 40%, C 33%,CN: 27%, LL: 27%, S: 9%
3C19	Blackhull, awnless, red pericarp (aus-like)
	Genotype description	Hull characteristic2
1C24	0-100: 0% aus and 100% indica (indica-like)1	Strawhull awnless
3C20	20-80: 18% aus and 82% indica (indica-like)1
2A2	50-50: 50% aus and 50% indica (admixed indica-aus)1	Brownhull awned
1C19	80-20: 79% aus and 21% indica (aus-like)1	Blackhull awnless
5C18	100-0: 98% aus and 2% indica (aus-like)1

• ¹Classification of Colombian weedy rice according to the predominant ancestry (> 80% of contribution) (Hoyos et al., 2020, 2019). ²Colombian weedy rice classification, BJ: Bajo Cauca; C: Centro; CN: Costa Norte; LL: Llanos; S: Santanderes (Hoyos et al., 2019).

Two mode of actions herbicides were tested. Glyphosate (EPSPS inhibitor; Roundup Activo^®, Compañía Agricola Colombiana LTDA) was evaluated at a commercial dose of 2.6 L ha^-1 (1,180 g a.i. ha^-1 of N-(Phosphonomethyl) glycine, 960 g a.e. ha^-1). The premix of imazamox + imazapyr (ALS inhibitors, Euroligthing^®, BASF Química Colombiana S.A) was tested at a dose of 1.5 L ha^-1 (49.5 + 22.5 g a.i. ha^-1, respectively). The treatments were applied at 3–4 leaves (V₃-V₄) for all weedy rice genotypes and morphotypes. We used the commercial rate to screen potential resistance, considering that populations that were no longer controlled by the commercial doses were resistant.

The response of the five morphotypes and the five genotypes to herbicides, including the rice cultivar, was assessed in separate experiments. Each experiment was conducted as a two-factor factorial (6 morphotypes or genotypes [including cultivar] x 3 herbicide treatments [including non-treated control]) randomized block design with three replications. Each replication had six plants per pot and the experiment was repeated in time. The six levels of the first factor included the rice cultivar Fedearroz-2000. The three levels of the second factor included the non-treated check.

Control (%) was evaluated at 7, 14, and 21 days after application (DAA) based on overall foliar damage and reduction of size compared to the non-treated, where 100% is dead and 0% is no visible effect. Mortality (%) was evaluated at 7, 14, and 21 DAA, calculating the proportion of dead plants relative to the number of plants sprayed. Shoot fresh biomass was recorded at 21 DAA using a precision balance (Denver instruments XE-100).

Analysis of variance was conducted, and the data were transformed as appropriate to achieve normal distribution of variance after examining plots of residuals. The effect of repetition was not significant, so the data from two runs of the experiments were pooled. When significant factor effects were detected, means were compared using Tukey’s test (p-values < 0.05) or control and shoot fresh biomass, and least significant difference test F-LSD (p-values < 0.05) for mortality. Statistical analyses were performed using the R^® version 3.5.2 GUI 1.70 statistic platform (R Core Team, 2024).

2.3 Baseline sensitivity of Colombian weedy rice genotypes to the premix of imazamox + imazapyr

The same five Colombian weedy rice genotypes previously described (Table 1) and the rice cultivar Fedearroz-2000 were sprayed with F-IMIs at seven increasing doses at V₃-V₄ growth stage. A randomized block experiment in a factorial scheme (6 x 7) with four replications was established and repeated over time. The six levels of the first factor corresponded to five weedy rice genotypes and the rice cultivar. The seven levels of the second factor were the herbicide rates 0, 0.15, 0.25, 0.5, 0.75, 1, 2 times the label rate of imazamox + imazapyr (49.5 and 22.5 g a.i. ha^-1, respectively). The dose range below the commercial rate was chosen considering the results from the first assay and to detect differential response to sublethal doses which may show elevation in background tolerance, indicative of possible introgression of CL rice resistance gene or resistance evolution across various generations of weedy rice. Dry shoot biomass and weed control (%) were recorded at 28 DAA, harvested shoots were dried in a forced-air oven (Binder ED56) for 48 h at 60 °C and weighed using a precision balance. Data were processed and analyzed following the same approach previously described. The effects of repetition and its interaction with treatments were not significant, thus the data were pooled across repetitions in the analysis.

The dose that reduces the growth by 50% (GR₅₀) was determined using the dry shoot biomass and the effective dose that controls the population 50% (ED₅₀) was determined using the control values. Regression parameters were determined for each population using a log-logistic model (Equation 1) of the drc package in R^® version 3.5.2 GUI 1.70 statistic platform (R Core Team, 2024; Ritz et al., 2015).

$y=f\left(x\right)=C+\frac{D-C}{1+\exp \left(b\right(\log \left(x\right)-\log \left(e\right)\left)\right)}$

In this model, C is the lower limit; D is the upper limit; b is the slope of the curve around e; and e is the rate of herbicide that results in 50% value of the response variable y (GR₅₀ or ED₅₀). The growth reduction relative to the non-treated check was used for the visualization figure. The four-parameter model was selected as the best fit based on the lesser log likelihood value using the mselect function in the drc package. The e values were compared using the EDcomp function of the drc package. EDcomp function compares e (ED₅₀ or GR₅₀) means using t-statistics, where p-value < 0.05 indicates significant differences between e values.

2.4 Weedy rice resistance level to the premix of imazamox + imazapyr

A strawhull-awned weedy rice morphotype (putative resistant, based on the results of the previous experiment section 2.2: R) and rice cultivar Fedearroz-2000 (susceptible check: S), were treated with seven doses of the F-IMIs at V₃-V₄ growth stage. A randomized block experiment in a factorial treatment scheme (2 x 7) with four replications was established and repeated over time. The two levels of the first factor were the R and S populations, and the seven levels of the second factor were the herbicide doses. The doses were 0, 0.5, 1, 2, 4, 8, and 16 times the commercial rate of F-IMIs (imazamox + imazapyr, 49.5 and 22.5 g a.i. ha-1, respectively) for the R population. The 0.15, and 0.25 times the commercial rate were included for the S population. Control (%) was evaluated at 28 DAA using the same scale as described above. Shoot biomass was collected at 28 DAA, dried in a forced-air oven (Binder ED56) for 48 h at 60 °C, and weighed using a precision balance. No significant differences were detected between repetitions over time, so the data were pooled.

The dose that reduces the growth by 25% (GR₂₅) was determined using the dry shoot biomass and the effective dose that controls the population by 25% (ED₂₅) was determined using the control values. The 25% cut off was chosen to assess differences between populations since the maximum reduction in biomass of the R population was 26%. The model does not fit for prediction of ED₂₅ of the R population. The corresponding regression parameters were determined using a log-logistic model (Equation 1). Comparisons of e values and model selection were done as described previously. Resistance index was determined by dividing the e value of strawhull-awned morphotype by the e value of Fedearroz-2000.

3.Results and Discussion

3.1 Differential response of weedy rice to the premix of imazamox + imazapyr and glyphosate

3.1.1 Colombian weedy rice response to glyphosate

Rice cultivar (Fedearroz-2000) and Colombian weedy rice morphotypes were equally susceptible to glyphosate, being controlled at above 90% at all the evaluation times (Table 2). The weedy rice genotypes differed in susceptibility to glyphosate at 7 DAA, with the indica-like (0–100) genotypes showing 75% control and the admixed indica-aus (50:50) genotype showing 58% control. Weedy rice control increased on average to 89% (range 82% to 95%) at 14 DAA and 95% (range 91% to 98%) at 21 DAA, such that differences between genotypes were no longer apparent (Table 2). The activity of glyphosate on morphotypes was faster than in the genotypes experiment reaching 100% efficacy. Glyphosate activity on the genotypes tested was slower and the maximum efficacy was 98%. Such differences between experiments were consistent across runs and could be due to slight variation in environmental conditions between the greenhouses where each experiment was conducted. Regardless, glyphosate reduced the fresh shoot biomass of all morphotypes and genotypes relative to their respective non-treated checks and the shoot biomass of treated plants were similar across morphotypes and genotypes (Table 3).

Table 2
Control level of Colombian weedy rice accessions (morphotypes or genotypes) to applications of glyphosate or premix of imidazolinones (imazamox + imazapyr).

Weedy rice accession	Control (%)1
	GLY2						F-IMIs3
	7DAA4		14DAA		21DAA		7DAA		14DAA		21DAA
Morphotypes5
SH-awned3	97.2	Aa	99.9	Aa	100.0	Aa	0.0	B c	0.0	Bc	0.0	Bb
SH-awnless	94.8	Aa	99.1	Aa	100.0	Aa	43.9	Bb	75.7	Bb	90.4	Ba
Br-awned	92.0	Aa	99.3	Aa	99.9	Aa	50.4	Bb	63.8	Bb	92.9	Aa
BH-awnless	96.8	Aa	99.6	Aa	100.0	Aa	40.9	Bb	77.2	Bab	91.5	Aa
BH-awned	90.6	Aa	99.3	Aa	100.0	Aa	56.8	Bb	80.3	Bab	93.6	Aa
F2000	94.8	Aa	99.3	Aa	99.9	Aa	88.6	Aa	92.8	Aa	97.8	Aa
Genotypes6
0-100	75.0	Aa	81.6	Aa	91.1	Aa	27.4	Ba	70.4	Ab	83.4	Aa
20-80	69.6	Aab	95.0	Aa	98.0	Aa	24.3	Ba	78.9	Ba	74.9	Ba
50-50	58.1	Ab	87.1	Aa	94.4	Aa	28.3	Ba	80.7	Aa	79.9	Aa
80-20	66.3	Aab	90.6	Aa	95.2	Aa	24.2	Ba	78.7	Aa	71.7	Ba
100-0	71.1	Aab	93.1	Aa	97.8	Aa	37.9	Ba	89.5	Aa	86.9	Aa

• ¹Control levels followed by the same capital letter for a particular morphotype or genotype within an evaluation time do not differ significantly. Morphotypes or genotypes followed by the same low case letter do not differ significantly in their response to each herbicide within a specific evaluation time. (Tukey multiple comparisons of means test with 95% confidence level). ²GLY: glyphosate (960 g a.e. ha^-1). ³F-IMIs: formulated mixture of imazamox plus imazapyr (49.5 and 22.5 g a.i. ha^-1, respectively). ⁴DAA: days after application. ⁵SH: strawhull, Br: brownhull BH: blackhull. ⁶Ancestry according to the aus-indica mixture (e.g., 0-100 represent 0% aus and 100% indica then considered indica-like).

Table 3
Effect of glyphosate and formulated mixture imidazolinones (imazamox + imazapyr) applications on fresh shoot weight of Colombian weedy rice morphotypes and genotypes evaluated at 21 days after treatment.

Weedy rice accession	Fresh shoot weight (g plant-1)1
	GLY2		F-IMIs3		Non-treated
Morphotypes4
SH-awned	0.06	Bns	4.29	Aa	4.52	Ans
SH-awnless	0.06	B	0.20	Bb	3.57	A
Br-awned	0.08	B	0.22	Bb	3.70	A
BH-awnless	0.07	B	0.22	Bb	4.03	A
BH-awned	0.08	B	0.23	Bb	4.10	A
F2000	0.07	B	0.14	Bb	4.10	A
Genotypes5
0-100	0.10	Cns	0.12	Bns	3.52	Ans
20-80	0.09	C	0.26	B	3.28	A
50-50	0.13	C	0.30	B	3.44	A
80-20	0.13	C	0.24	B	3.60	A
100-0	0.12	C	0.19	B	3.44	A

• ¹Capital letters represents significant difference between active ingredients and non-treated check. Lowercase letters represent significant difference within morphotypes or within genotypes (Tukey multiple comparisons of means test with 95% confidence level). ns: non-significative differences within morphotypes or within genotypes. ²GLY: glyphosate (960 g a.e. ha^-1). ³F-IMIs: formulated mixture of imazamox plus imazapyr (49.5 and 22.5 g a.i. ha^-1, respective). ⁴SH: straw-hulled, Br: brown-hulled BH: black-hulled. ⁵Ancestry according to the aus-indica mixture (e.g., 0-100 represent 0% aus and 100% indica then considered indica-like).

The weedy rice morphotypes and genotypes were all more sensitive to glyphosate than they were to the F-IMIs. At 21 DAA, the morphotypes and genotypes averaged 98.6% and 94.5% mortality, respectively, with the glyphosate treatment (Table 4). Conversely, only 16.7% and 57.8% were killed by the F-IMIs, respectively (Table 4).

Table 4
Effect of glyphosate and formulated mixed imidazolinones (imazamox + imazapyr) applications on mortality of Colombian weedy rice morphotypes and genotypes.

Treatment	Mortality (%)
	Morphotypes						Genotypes
	7 DAA1		14 DAA		21 DAA		7 DAA		14 DAA		21 DAA
GLY2	0.0	(0.0)4	62.5	(45.2)	98.6	(60.6)	0.0	(0.0)	64.5	(34)	94.5	(13.9)
F-IMIs3	0.0	(0.0)	6.5	(1.6)	16.7	(7.6)	0.0	(0.0)	17.8	(4)	57.8	(40.3)
LSD50.05	ns		13.8		19.4		ns		11.4		13.1

• ¹DAA: days after application. ²GLY. glyphosate (960 g a.e. ha^-1). ³F-IMIs. formulated mixture of imazamox plus imazapyr (49.5 and 22.5 g a.i. ha^-1, respective). ⁴Numbers within parenthesis are standard deviation (n=6). ⁵Fisher Protected Least Significant Difference (LSD) test at 0.05 significant level, for mortality level across herbicides within an evaluation time, ns: non-significative differences.

Similar responses were observed among weedy rice accessions collected sequentially in 2002 to 2003 and 2008 to 2009 from major rice-growing counties of Arkansas, USA (Roma-Burgos et al., 2011; Shrestha et al., 2019). In the first study glyphosate (900 g a.e. ha^-1) controlled the straw-hulled, black-hulled, and brown-hulled weedy rice accessions in the range of 81–100% regardless of application timing. In the second sequential study 1,120 g a.e. ha^-1 glyphosate provided 70% to 98% control of weedy rice except three accessions (B2, B20, and S11) which had 36% control and resistance ratios of 3.3, 4.0, and 8.3, respectively (Shrestha et al., 2019). In contrast to our results, Shrestha et al. (2019) reported poor control of blackhull accessions from Arkansas, USA (74% and 76%, at 21 and 35 DAA, respectively) with glyphosate. It is believed that control below 90% is indicative of a risk for resistance evolution should the selection pressure with glyphosate on weedy rice intensify (Roma-Burgos et al., 2011; Shrestha et al., 2019). The blackhull weedy rice accessions from Colombia exhibited 90% and 100% control with glyphosate at 7 and 21 DAA, respectively.

In Brazil, some growers apply glyphosate to rice at the spiking stage (S3) to control weeds that had emerged ahead of rice, including weedy rice (Cassol et al., 2015; Menezes et al., 2013). Applying glyphosate in this manner at 1,200 g a.e. ha^-1 can reduce weedy rice infestation by 75% (Menezes et al., 2013).

Due to the high efficacy of glyphosate (99–100% control) on Colombian weedy rice at the label rate of 960 g a.e. ha^-1, and the similarity in response between morphotypes and genotypes, we reject the hypothesis that Colombian weedy rice populations have differential tolerance to glyphosate. Therefore, glyphosate can be used as part of an integrated weed management plan to mitigate the evolution of resistance. We recommended to manage the potential evolution of resistance of weedy rice to glyphosate by crop and herbicide mode of action rotation to avoid constant selection pressure. It has been documented that weedy rice plants that survive a full dose of glyphosate (900 g a.e. ha^-1) can produce viable seeds (30–100% of accessions) (Roma-Burgos et al., 2011). Seeds of survivors have similar germination capacity regardless of hull color (Roma-Burgos et al., 2011). However, it is important to consider that the weedy rice survivors from our recent study in Colombia were highly injured (99%); these plants would not be able to compete with other plants in the field and the probability of seed production would be nil.

At a dose of 450 g a.e. ha^-1 glyphosate (0.5X of field dose) 46–64% of surviving accessions in Arkansas, USA did not produce seeds; sterile survivors increased to 76-79% at the full dose of glyphosate (Roma-Burgos et al., 2011). Using the proper rate minimizes seed production from survivors. Although seed production from survivors was not quantified in our study in Colombia, we should not overlook the low proportion of survivors (1.6%–5.5%) from glyphosate application despite the high level of injury. It is necessary to use glyphosate at proper rate (Colombia ful ratel: 900 g a.e. ha^-1), avoid sublethal application due to poor spray overlap, add adjuvants that increase absorption (such as sulfate ammonium), perform cultural practices to ensure suppression of highly injured weedy rice survivors, and prevent seed production.

3.1.2 Colombian weedy rice response to the premix of imazamox + imazapyr

Four of the five weedy morphotypes tested were susceptible to F-IMIs, exhibiting > 90% control 21 DAA (Table 2). The strawhull-awned morphotype did not exhibit any visible effect (0% injury) with the full dose used (imazamox + imazapyr 49.5 and 22.5 g a.i. ha^-1, respectively). The fresh shoot biomass of this putative resistant morphotype was not reduced by F-IMIs, whereas shoot biomass of the other morphotypes was reduced relative to their corresponding nontreated checks (Table 3). To determine if the response of the strawhull-awned morphotype is typical, another five accessions of the same morphotype were treated with the full rate of F-IMIs in a follow-up experiment. The response was similar to that of the susceptible morphotypes, with control ratings > 90% (data not shown). We therefore conclude that the insensitivity of the one strawhull-awned accession is atypical of other populations of the same morphotype. This putative IMI-resistant accession was collected from a major rice production zone in the Norte de Santander region, which has a history of CL rice production. In early 2010, farmers and agronomists mentioned planting CL rice seed from Venezuela in some areas of Santander (Saldain, 2011).

The five genotypes tested responded similarly to F-IMIs across evaluation times. In this experiment, F-IMIs controlled the genotypes 24% to 37%, 70% to 89% and 71% to 86% at 7, 14 and 21 DAA, respectively (Table 2). The indica-like accession 0–100 had the lowest control at 14 DAA compared to the rest of accessions. The F-IMIs similarly reduced the shoot biomass collected at 21 DAA of all genotypes relative to the non-treated check (Table 3). These genotypes were selected based on the five most representative ancestry groups of weedy rice from Colombia (Hoyos et al., 2019). We hypothesized that ancestry of this group is not a determinant of Colombian weedy rice response to F-IMIs. To test this hypothesis, we evaluated the effect of increased rates of F-IMIs on weedy rice genotypes with different genetic ancestry (see section 3.2).

As mentioned before, the F-IMIs was less effective than glyphosate on controlling weedy rice (Table 2 and Table 4). However, the maximum efficacy of F-IMIs might not have been manifested at 21 DAA as mortality and control percentage increased between 14 and 21 DAA. Thus, evaluation time for F-IMIs was extended to 28 DAA in subsequent experiments.

Data herein support that the CL rice technology is still useful in selectively controlling weedy rice in Colombia, provided that these herbicides are used in addition to, and in rotation with, other herbicides with different modes of action. One basic stewardship practice is to reduce the weedy rice population by preplant tillage and application of burndown herbicide (i.e. glyphosate) to the first cohort of emerged weedy rice. Alternatively, the burndown herbicide application can be omitted, and a second tillage can be done instead to kill emerged weedy rice.

3.2 General sensitivity of Colombian weedy rice genotypes to the premix of imazamox + imazapyr

To test the hypothesis that Colombian weedy rice genotypes differ in sensitivity to the F-IMIs, a dose-response experiment was conducted. The five weedy rice genotypes tested were susceptible to F-IMIs, and the dose required to reduce shoot biomass by 50% (GR₅₀) was around 0.3 times the label rate, confirming results of previous experiment (Figure 1a). The sensitivity index based on GR₅₀ ranged from 18.92 to 23.38 g a.i. ha^-1 (Table 5). Similarly, the ED₅₀ value was around 0.3 the label doses (Figure 1b) and the resultant sensitivity index ranged from 0.81 to 0.97 (Table 5).The ED₅₀ suggested more susceptibility of the admixed accession (50–50, aus -Indica) compared to the susceptible cultivar (Table 5). In this study, the 50–50 aus-indica weedy rice genotype appeared more susceptible to F-IMIs than the standard susceptible rice cultivar. It was also apparent that the ancestry of weedy rice does not play a role in the evolution of resistance to F-IMIs.

Figure 1
Modeled dose-respond of growth reduction (a) and control (b) of five Colombian weedy rice genotypes with variable ancestry (aus-indica percent content) and rice susceptible variety (Fedearroz 2000) in response to formulated mixture of imazamox + imazapyr application (2.2:1 ratio, respectively) 28 days after application. Values are the average for four reps consolidated from two runs separated in time.

Table 5
Parameter estimates of the regression equation used to calculate the herbicide dose required for growth reduction by 50% (GR50) and control to 50% (ED50), 28 days after application for five Colombian admixed indica-aus weedy rice genotypes and rice susceptible variety (F2000) in response to formulated mixture of imazamox + imazapyr.

Genotype	b1	c2	d3	GR50				Susceptibility ratio5	P-value6
				e (g a.i. ha-1)4		(95% CI)
F2000	7.30	0.23	2.08	20.74	16.11		25.36	-	-
100-0 (aus-like)	3.60	0.16	2.27	19.16	15.68		22.63	0.92	0.572
80-20 (aus-like)	9.55	0.23	1.87	23.38	13.18		33.58	1.13	0.649
50-50 (indica-aus)	12.06	0.12	1.32	19.32	7.30		31.35	0.93	0.827
20-80 (indica-like)	12.56	0.17	1.75	18.92	13.93		23.90	0.91	0.583
0-100 (indica-like)	8.50	0.23	1.84	21.29	11.78		30.79	1.03	0.919
ED50
F2000	-6.51	2.18	96.79	23.09	21.04		25.14	-	-
100-0 (aus-like)	-3.85	6.66	95.91	22.40	20.64		24.17	0.97	0.611
80-20 (aus-like)	-93.64	6.30	87.56	18.79	6.82		30.75	0.81	0.483
50-50 (indica-aus)	-54.15	2.19	91.13	18.34	16.79		19.90	0.79	5.4E-05
20-80 (indica-like)	-5.71	3.03	95.90	21.82	20.03		23.62	0.95	0.344
0-100 (indica-like)	-36.17	4.67	96.12	19.04	9.55		28.53	0.82	0.408

• ¹Slope around GR₅₀ and ED₅₀. ²Lower limit for all plants (g for GR₅₀ and % for control for ED₅₀). ³Upper limit for all plants (g for GR₅₀ and % for control for ED₅₀). ⁴ Rate of formulate mix imazamox + imazapyr (2.2:1 ratio, respectively) that causes GR₅₀ and ED₅₀. ⁵Susceptibility ratio = GR₅₀ genotype/GR₅₀ F2000 or ED₅₀ genotype/ED₅₀ F2000. ⁶F2000 vs. each genotype t-statics comparison of GR₅₀ or ED₅₀, p-value<0.05 means significand difference between e.

Regarding the sensitivity of Colombian weedy rice genotypes to F-IMIs, similar results have been reported in whole plant experiments, where a susceptible red rice accession (MS5) to imazethapyr was detected, with a susceptibility index of 0.5 (6.9 g a.i. ha^-1) compared with a susceptible cultivar (Cypress) (Avila et al., 2005). These authors evaluated the response of both accessions to ALS herbicide and did not detect any difference. The authors posited that any level of differential tolerance could be due to differential metabolism, absorption or translocation. Therefore, the slight difference in susceptibility of Colombian weedy rice to F-IMIs is also most likely due to background differences in these mechanisms.

Preventing the evolution of resistance to herbicides used in herbicide-resistant rice must be a priority. We encourage strengthening the education and outreach efforts for agronomists, technicians, farmers, and agricultural product dealers with respect to stewardship of crop production technologies.

3.3 Weedy rice resistance level to the premix of imazamox + imazapyr

A dose-response experiment was conducted to determine the resistance level of the putative resistant strawhull-awned accession to F-IMIs. The rate of imazamox + imazapyr that reduced shoot biomass by 25% of the susceptible cultivar was about 2.5-fold the label rate of this mixture (GR₂₅: 17.5 g a.i. ha^-1). In contrast, the GR₂₅ for the putative resistant strawhull-awned accession were more than 11 times the label rate (821.34 g a.i. ha^-1) (Figure 2 and Table 6). Thus, we confirmed resistance of this strawhull-awned accession to F-IMIs (resistant index: 47-fold times, based on GR₂₅). The log-logistic model could not be used to analyze the level of control of the strawhull-awned accession (p-value: 0.334) due to the low level and high variability. Nevertheless, the ED₂₅ for the susceptible accession was 21.35 g a.i. ha^-1 (Table 6).

Figure 2
Modeled dose-response of growth reduction of strawhull-awned weedy rice morphotype (SH-awned) and the susceptible rice variety (Fedearroz 2000) in response to the premix of imazamox + imazapyr (2.2:1 ratio, respectively) 28 days after application. Values are the average for four reps consolidated from two runs separated in time. Error bars exhibit the confidential interval 95%.

Table 6
Parameters estimate of the regression equation used to calculate the herbicide dose required for reduction growth to 25% (GR25) and control to 25% (ED25), 28 days after application for Colombian weedy rice straw-hulled-awned (SH-awned) morphotype and rice cultivar Fedearroz 2000 (susceptible) in response to formulate mixture of imazamox + imazapyr.

Population	b1	c2	d3	GR25			Resistance ratio5	P-value 6
				e (g a.i. ha-1)4	(95% CI)
Susceptible	6.18	0.20	1.06	17.46	12.10	22.83	-	-
SH-awned	0.98	2.08	2.81	821.34	177.92	1464.76	47.04	0.023
ED25
Susceptible	-7.50	0.24	86.12	21.35	16.59	26.12
SH-awned	NA	NA	NA	NA	NA	NA	NA	NA

• ¹Slope around. ²Lower limit for all plants (g for growth reduction and % for control). ³Upper limit for all plants (g for growth reduction and % for control). ⁴Rate of formulate mix imazamox + imazapyr (2.2:1 ratio, respectively) that causes GR₂₅ and ED₂₅. ⁵Resistance ratio = GR₂₅ SH-awned/ GR₂₅ Susceptible. ⁶Suceptible vs. Sh-awned t-statics comparison of GR₂₅, p-value<0.05 means significand difference between e. NA: not adjusted to log-logistic model.

Resistance to IMI herbicides in weedy rice has evolved in regions where CL rice is produced primarily due to gene flow. In Brazil, for example, 27.8% of farmers reported poor efficacy on weedy rice (less than 60%) after 20 years of adopting the CL system, due to the evolution of IMI-resistant weedy rice (Avila et al., 2021b). Even with this reduced level of efficacy, farmers are still planting CL (82.2% of respondents in Rio Grande do Sul) mainly due to the lack of other options to manage weedy rice. A survey in Arkansas, USA, and adjacent locales showed split opinions among respondents, where 37.5% considered high efficacy on weedy rice (> 90%), while the same number of respondents reported moderate to low efficacy (< 70%) (Roma-Burgos et al., 2021a). More options for weedy rice management such as rice rotation with soybean (58% of respondents rotating CL rice) in the USA most likely contributed to the preservation of the efficacy of CL system in the USA, compared to Brazil where only 35% of respondents practiced crop rotation with CL rice. In Italy, 46.9% of farmers surveyed used imazamox-resistant CL rice to control weedy rice, from which 65% reported resistance of weedy rice to this herbicide (Ferrero et al., 2021). In tropical regions, the evolution of IMI-resistant weedy rice is exacerbated. In Malaysia, for example, conditions allow rice producers to plant up to five cycles of rice in two years, and the absence of winter-killing of weedy rice seeds allows continuous selection pressure in weedy rice populations (Ruzmi et al., 2021).

Resistance levels vary from 3.5- to 4.5-fold in Brazil (Cassol et al., 2015); 50- to 67-fold in Malaysia (Dilipkumar et al., 2018) for the mixture of imazapic plus imazapyr; from 86.4- to 147-fold for imazamox and imazethapyr, respectively, in Greece (Kaloumenos et al., 2013); and 6.3 to 25.7 for imazapyr; and from 9 to 21.4 for imazamox, in USA (Kuk et al., 2008). In almost 100% of cases, resistance is due to gene flow (Avila et al., 2021b; Ferrero et al., 2021; Roma-Burgos et al., 2021a). With gene flow, the resulting resistant outcrosses carry the target site mutations from the herbicide-resistant rice including Gly-654-Glu, Gly-654-Asn, Ser-653-Asn and, Ala-112-Thr (Roso et al., 2010; Wedger et al., 2022). These mutations confer broad cross-resistance to IMI herbicides as has been documented in a weedy rice population from the USA with cross-resistance to imazaquin, imazamox, imazapyr and imazethapyr (Kuk et al., 2008).

Weedy rice resistance to premixed IMIs herbicides have been described in Malaysia (Dilipkumar et al., 2018; Ruzmi, Mazlan, 2020) and Brazil (Cassol et al., 2015; Goulart et al., 2016; Roso et al., 2010). Generally, it has been shown that gene flow from CL cultivars is responsible for this herbicide-resistance evolution rather than de novo mutations (Ruzmi, Mazlan, 2020).

On rare occasions, resistance to IMI herbicides in weedy rice has evolved due to selection of standing variation (Sales et al., 2008; Wedger et al., 2022). The resistance-conferring ALS mutation Gly-654-Glu has been documented in a US weedy rice population sampled before the commercialization of CL rice (Sales et al., 2008). Likewise, resistance to IMIs or other ALS herbicides in weedy rice can be conferred by nontarget-site resistance mechanisms as indicated by the presence of resistant plants without resistance-conferring ALS mutations (Wedger et al., 2022).

In Colombia gene flow from IMI-resistant rice cultivar to weedy rice has been studied, under controlled conditions, estimating a range of 0.03% to 0.36% of outcrossing (Velasquez et al., 2007). The weedy rice previously studied contained the mutation Gly-654-Glu from CL-205 rice; survivors from these populations exhibited about 50–98% control 35 DAA imazapic (140 g a.i. ha^-1) in field conditions (Velasquez et al., 2007). CL-205 was not broadly adopted by farmers in early 2000s due to low tolerance to the recommended IMI rate (imazapic) and susceptibility to white leaf virus (Saldain, 2011). Therefore, before this research, full resistance (47-fold resistance index) to premixed IMI herbicides in a field population of weedy rice in Colombia has not been documented.

The phenological evaluation conducted in Colombia showed that the weedy rice morphotypes and genotypes did not differ in flowering time from the rice cultivars (Hoyos et al., 2019). Thus, this synchronization in flowering between crop and weed increases the probability of gene flow. The strawhull-awned morphotype is the most common weedy rice type in rice-producing areas in Colombia (47%) as well as in the Norte de Santander department (64%) where the confirmed ALS-resistant weedy rice accession was collected (Hoyos et al., 2019). The CL technology has been adopted in Colombia rice areas for more than a decade (Saldain, 2011; Sudianto et al., 2013). We hypothesized that resistance to IMI herbicides in the Colombian weedy rice population is due to gene flow; however, it is also possible that de-novo mutations or other resistance mechanisms have been selected as documented among current weedy rice populations in fields with a history of CL rice (Wedger et al., 2022). This can be resolved with follow-up experiments to determine the existence of target site mutation(s) and its origin. Further investigations should focus on elucidating the resistance mechanisms of Colombian weedy rice to IMIs.

4.Conclusions

The Colombian weedy rice populations tested are susceptible to glyphosate. In general, these populations are also susceptible to the formulated mixture of imazamox + imazapyr. One accession of a strawhull-awned morphotype is highly resistant to the formulated mixture of imazamox + imazapyr.

The weedy rice genotypes of various ancestry do not differ in susceptibility to the formulated mixture of imazamox + imazapyr. Further research activities should focus on monitoring the occurrence of resistance among the Colombian weedy rice populations and developing better weed management strategies.

Acknowledgements

The authors acknowledge to all persons who participated directly or indirectly in the development of this project. The authors acknowledge the assistance from Maria del Mar Vanega, Daniela Cardenas, Laura Rodríguez and Catalina Rodríguez. This research was supported by project No. 35024 “Variabilidad fenotípica de arroz maleza colombiano” at the Universidad Nacional de Colombia, Bogotá D.C.

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• Funding:
  Project No. 35024 “Variabilidad fenotípica de arroz maleza Colombiano” at the Universidad Nacional de Colombia, Bogotá D.C.

Edited by

• Editor in Chief:
  Carol Ann Mallory-Smith

• Associate Editor:
  André da Rosa Ulguim

Publication Dates

• Publication in this collection
  17 Jan 2025
• Date of issue
  2024

History

• Received
  2 June 2024
• Accepted
  5 Nov 2024