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.2014 Nov;166(3):1177-85.
doi: 10.1104/pp.114.241950. Epub 2014 Jul 30.

Indaziflam herbicidal action: a potent cellulose biosynthesis inhibitor

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Indaziflam herbicidal action: a potent cellulose biosynthesis inhibitor

Chad Brabham et al. Plant Physiol.2014 Nov.

Abstract

Cellulose biosynthesis is a common feature of land plants. Therefore, cellulose biosynthesis inhibitors (CBIs) have a potentially broad-acting herbicidal mode of action and are also useful tools in decoding fundamental aspects of cellulose biosynthesis. Here, we characterize the herbicide indaziflam as a CBI and provide insight into its inhibitory mechanism. Indaziflam-treated seedlings exhibited the CBI-like symptomologies of radial swelling and ectopic lignification. Furthermore, indaziflam inhibited the production of cellulose within <1 h of treatment and in a dose-dependent manner. Unlike the CBI isoxaben, indaziflam had strong CBI activity in both a monocotylonous plant (Poa annua) and a dicotyledonous plant (Arabidopsis [Arabidopsis thaliana]). Arabidopsis mutants resistant to known CBIs isoxaben or quinoxyphen were not cross resistant to indaziflam, suggesting a different molecular target for indaziflam. To explore this further, we monitored the distribution and mobility of fluorescently labeled CELLULOSE SYNTHASE A (CESA) proteins in living cells of Arabidopsis during indaziflam exposure. Indaziflam caused a reduction in the velocity of YELLOW FLUORESCENT PROTEIN:CESA6 particles at the plasma membrane focal plane compared with controls. Microtubule morphology and motility were not altered after indaziflam treatment. In the hypocotyl expansion zone, indaziflam caused an atypical increase in the density of plasma membrane-localized CESA particles. Interestingly, this was accompanied by a cellulose synthase interacting1-independent reduction in the normal coincidence rate between microtubules and CESA particles. As a CBI, for which there is little evidence of evolved weed resistance, indaziflam represents an important addition to the action mechanisms available for weed management.

© 2014 American Society of Plant Biologists. All Rights Reserved.

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Figures

Figure 1.
Figure 1.
Indaziflam is a fluoroalkytriazine-containing compound that inhibits elongation in seedlings ofP. annua and Arabidopsis. A, Chemical structure of indaziflam. B to D, Images of 7-d-old seedlings treated with increasing concentrations of indaziflam. B shows light-grownP. annua seedlings (indaziflam concentrations from left to right are 0, 100, 250, 500, 1,000, 5,000, and 10,000 pm). C and D show light-grown and dark-grown Arabidopsis seedlings, respectively (indaziflam concentrations from left to right are 0, 100, 250, 500, 1,000, and 2,500 pm). Indaziflam treatment induced swollen cells. E, Representative images of the primary root ofP. annua grown in plates for 4 d with and without 10 nm indaziflam. F, Transgenic Arabidopsis seedlings expressing GFP:PIP2 were examined by laser scanning confocal microscopy and images represent visualization of the primary root grown vertically for 7-d plates without and with 250 pm indaziflam. PIP2, Plasma membrane intrinsic protein2. Bar = 10 mm in B, 5 mm in C and D, 2 mm in E, and 50 μm in F.
Figure 2.
Figure 2.
Indaziflam treatment quantitatively inhibited the production of cellulose. A, The amount of acid-insoluble Glc content (crystalline cellulose) from pooled etiolated hypocotyl regions (5 mg of dry weight) of 5-d-old dark-grown Arabidopsis seedlings after treatment with indaziflam at 0 (0.01% DMSO mock), 200, or 400 pm. B, The inhibitory effects of indaziflam on the incorporation of [14C]Glc into the acid-insoluble cellulose fraction of 3-d-old etiolated dark-grown Arabidopsis seedlings after a 1-h treatment. The amount of radioactivity was determined by liquid scintillation spectrometry. In graphs, means were separated using Tukey’s test (A) or a Student’st test (B) and different letters or asterisks indicate a significant difference at an α < 0.05. Error bars represent ±1se (n = 5 for A and B). DPM, Disintegrations per minute.
Figure 3.
Figure 3.
Indaziflam dose response and GR50 values of light-grown Arabidopsis genotypes. To establish dose responses, seedlings were germinated in the light on agar plates containing indaziflam concentrations ranging from 0 to 10,000 pm. Seedling root length was measured and standardized as a percentage of the control. The Arabidopsis seedlings used in this assay were the Columbia ecotype as the wild type and mutants previously confirmed resistant to other CBIs. Thecesa3ixr1-1 andcesa3ixr1-2 mutants are resistant to isoxaben andcesa1ageusus is resistant to quinoxyphen. The curves and GR50 values were generated by R software using thedrc package. Asterisks indicate a significant difference (n = 60;P < 0.05) in the GR50 values between the mutant and the wild type. [See online article for color version of this figure.]
Figure 4.
Figure 4.
Indaziflam treatment induced a higher density of CESAs at the PM. Arabidopsis seedlings expressing YFP:CESA6 were grown in the dark for 3 d before imaging. A, Representative images and analysis of the PM-localized YFP:CESA6 particles in theprc1-1 background are shown. Single optical sections (monochrome) show the distribution of YFP:CESA6-labeled puncta upon 2-h 0.01% DMSO mock treatment (left) or 500 nm indaziflam treatment (right). The green/magenta overlay is a spatial count of the puncta that display morphology and motility consistent with PM YFP:CESA6 particles. A gray mask indicates the region of interest lacking underlying intracellular compartments, and magenta dots indicate local maxima of the fluorescence signal. B, Upon indaziflam treatment, the average density of YFP:CESA6 puncta at the PM increased.n = 15 cells from nine seedlings for mock andn = 18 cells from 12 seedlings for indaziflam. Error bars are ±1se from the mean. Bar = 10 μm.
Figure 5.
Figure 5.
Indaziflam reduced the velocity (particle movement rate) of YFP:CESA6. A, Representative time-lapse images of YFP:CESA6 particles in theprc1-1 background with and without indaziflam treatment (61 frames averaged). B, The histogram depicts the frequency of YFP:CESA6 particle velocities at the PM focal plane after a 2-h treatment with indaziflam or DMSO mock. Velocity was determined from images taken in the epidermal cells of 3-d-old dark-grown hypocotyls. The white bars are the recorded velocity from the mock and the black bars are indaziflam treatment (mean ±1se). Bar = 10 μm
Figure 6.
Figure 6.
Indaziflam treatment decreased the net colocalization between MTs and YFP:CESA6 at the PM. Arabidopsis seedlings expressing both RFP:TUA5 and YFP:CESA6 inprc1-1 were grown in the dark for 3 d before imaging. Representative single optical sections (monochrome) of cortical MTs labeled by RFP:TUA5 (magenta) and PM-localized YFP:CESA6 (green) were used for the colocalization analysis (Table I). After 2 h in 0.01% DMSO mock, 71% ± 1% of YFP:CESA6 particles were coaligned with MTs, which was not different from the ratio without any treatment (Li et al., 2012). After 2 h in 500 nm indaziflam, the colocalization ratio between YFP:CESA6 and RFP:TUA5 decreased to 53% ± 4%, which was not significantly different from the expected random ratio association of 47% ± 10%. Bar = 5 μm.
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References

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