Low temperatures enhance the absorption and translocation of 14C-glyphosate in glyphosate-resistant Conyza sumatrensis

https://doi.org/10.1016/j.jplph.2019.153009Get rights and content

Abstract

Influence of low temperatures on the glyphosate efficacy was studied in glyphosate-resistant (R) and -susceptible (S) Conyza sumatrensis biotypes. For this purpose, the physiological and enzymatic aspects involved were characterized under two growing temperature regimes [high (30/20 °C) and low 15/5 °C temperatures day/night]. The R biotype was 5.5 times more resistant than the S biotype at high temperatures; however, this R-to-S ratio decreased to 1.6 at low temperatures. At 96 h after treatment (HAT), the shikimic acid accumulation was higher in the S biotype in both temperature regimes (4.6 and 1.9 more shikimic acid at high and low temperatures, respectively), but the accumulation of the R biotype increased 2.6 times at low temperatures compared to high ones. From 24 to 96 HAT, the 14C-glyphosate absorption ranged from 28 to 65% (percentage reached from 48 HAT) at low temperatures, and from 20 to 50% at high temperatures (gradual increase), but there were no differences between C. sumatrensis biotypes within each temperature regime. At high temperatures, the 14C-glyphosate translocation was different between biotypes, where the R one retained at least 10% more herbicide in the treated leaves than the S biotype at 96 HAT. So, the S biotype translocated 40% of 14C-glyphosate absorbed to roots, and the R biotype translocated only 28% of herbicide at the same period. At low temperatures, there were no differences between biotypes, and at 96 HAT, the 14C-glyphosate found in treated leaves was ˜47% and up to ˜42% reached the roots, i.e., the resistance mechanism was suppressed. The basal and enzymatic activities of the 5-enolpyruvyishikimate 3-phosphate synthase were different between temperature regimes, but there was no differences between biotypes within each temperature regime, showing that target-site resistance mechanisms did not contribute in the glyphosate resistance of the R biotype. Low temperatures enhanced the absorption and translocation of glyphosate by suppressing the resistance mechanisms improving its efficacy on resistant plants. This is the first characterization about the role of temperatures in the glyphosate efficacy on C. sumatrensis.

Introduction

The use of herbicides is increasing in worldwide crop production each year due, among other factors, to the reduction of workers for hand weeding (Gianessi, 2013). Indiscriminate use of herbicides, together with a lack of an integrated weed management have led to the appearance of weed biotypes resistant to herbicides in different cropping systems. A weed biotype resistant to a given herbicide is able to survive, complete its life cycle and reproduce by seed after application of the herbicide at a dose normally lethal for a wild biotype of the same species (Beffa et al., 2019). Herbicide resistance is one of the major concerns in the modern agriculture (Burgos et al., 2013), and worldwide, there are 255 species (148 dicots and 107 monocots) resistant to herbicides (Heap, 2019).

Glyphosate is a full spectrum herbicide that acts by inhibiting the enzyme 5-enolpyruvyishikimate 3-phosphate synthase (EPSPS), an important enzyme in the shikimate pathway for the biosynthesis of aromatic amino acids (Steinruecken and Amrhein, 1980). This herbicide has been used to control weeds in different crop situations such as citrus orchards, olive groves, and vineyards in southern Spain. However, biotypes of Conyza species (C. bonariensis, C. canadensis and C. sumatrensis) has been reported to be glyphosate resistant in this country (Urbano et al., 2007; González-Torralva et al., 2012, 2014; Amaro‐Blanco et al., 2018). Conyza spp. has evolved resistance to various herbicidal mechanisms of action (Kleinman and Rubin, 2017) such as ALS-inhibitors, paraquat, atrazine, and among other herbicides, with some populations evolving resistance to more than one herbicide mode of action (Heap, 2019).

Conyza sumatrensis (Retz.) E. Walker is an annual, biennial or perennial herbaceous plant native to South America (Buhler and Owen, 1997). It can be found in subtropical and temperate climates, is a very invasive weed because produces high amounts of achenes which are easily dispersed by wind (Hao et al., 2009). Conyza spp. have susceptibility differential to glyphosate with C. sumatrensis being the most susceptible (González-Torralva et al., 2010). Glyphosate resistant populations of Conyza spp. from several parts of the world has been described carrying target-site (TSR) and non-target-site (NTSR) resistance mechanisms, both isolated or associated (González-Torralva et al., 2012, 2014; Kleinman and Rubin, 2017; Page et al., 2018; Mei et al., 2018). Conyza spp. can exhibit high tolerance to glyphosate when treated at high temperatures or when plants are treated at advanced phenological stages (Shrestha et al., 2007; González-Torralva et al., 2010). However, there is evidence that environmental conditions, mainly the low temperatures (Vila-Aiub et al., 2013; Ghanizadeh et al., 2015a), may reduce the glyphosate resistance levels by suppressing the mechanism involved (Ge et al., 2011; Tani et al., 2016).

Temperature influences the glyphosate efficacy (Ghanizadeh et al., 2015a) and low temperatures can reduce the resistance levels by suppressing the NTSR mechanism involved (Ge et al., 2011). The aims of this research were a) to characterize the glyphosate efficacy through dose-response assays in a resistant (R) C. sumatrensis biotype in comparison to one susceptible (S); and b) to determine the physiological and enzymatic aspects (shikimic acid accumulation, absorption and translocation, and EPSPS activity assays), influencing the glyphosate under two temperatures regimes.

Section snippets

Plant material and temperature conditions

Two biotypes of C. sumatrensis (S and R) were used in all the experiments described below. Seeds of R biotype were collected from plants that survived glyphosate field doses (1080 g ae ha−1) used in a citrus area located in the Southern Spain (37º13’35.8”N 7º17’02.8”W). S seeds were harvested from a nearby area never treated with herbicide (37º14’15.2”N 7º16’38.0”W).

Seeds of both biotypes were sown in trays containing moistened peat and covered with transparent film until the emergence. Trays

Whole plant dose-response assays

The biotype R, grown at high temperatures (30/20 °C), showed the highest GR50 value (281.2 g ae ha−1), meanwhile this value was almost halved (GR50 = 152.1 g ae ha−1) at 15/5 °C (low temperatures). The susceptibility of the biotype S showed a GR50 value of 50.9 g ae ha−1 at high temperatures and increased to 94.3 g ae ha−1 at low temperatures. Thus, the proportion of resistance indexes (RI = R/S) decreased from 5.5 (high temperatures) to 1.6 (low temperatures) (Table 1, Fig. 1).

Shikimic acid accumulation

The presence of

Discussion

Results of this work demonstrated the selected resistance to glyphosate in the R biotype of C. sumatrensis in relation to the S biotype. Glyphosate efficacy is dependent on the temperature (Ghanizadeh et al., 2015a), as observed in this study when the response to glyphosate of the two S and R biotypes assessed was different depending to the growth temperature regime. By other hand, several studies highlight that the effectiveness of glyphosate is higher at high temperatures than low ones (

Conclusion

Control of some herbicide resistant weeds could be realized more efficiently if the herbicide is applied when low temperatures occurs, but previously knowledge on the physiology and biochemical basis of resistance are needed. Summarizing, as was demonstrated, the low temperatures enhanced the absorption and translocation of 14C-glyphosate in the glyphosate-resistant and-susceptible plants of C. sumatrensis showing a better efficacy of herbicide at low temperatures.

Acknowledgements

The authors thank to Rafael Roldan for his technical assistance in the growth chamber experiments. This study was financed by the grant AGL2016-78944-R (MINECO-Spain).

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