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Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules.

Chen X, Grandont L, Li H, Hauschild R, Paque S, Abuzeineh A, Rakusová H, Benkova E, Perrot-Rechenmann C, Friml J - Nature (2014)

Bottom Line: Here we show in the model plant Arabidopsis thaliana that in elongating cells exogenous application of auxin or redistribution of endogenous auxin induces very rapid microtubule re-orientation from transverse to longitudinal, coherent with the inhibition of cell expansion.This fast auxin effect requires auxin binding protein 1 (ABP1) and involves a contribution of downstream signalling components such as ROP6 GTPase, ROP-interactive protein RIC1 and the microtubule-severing protein katanin.These components are required for rapid auxin- and ABP1-mediated re-orientation of microtubules to regulate cell elongation in roots and dark-grown hypocotyls as well as asymmetric growth during gravitropic responses.

View Article: PubMed Central - PubMed

Affiliation: 1] Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria [2] Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie (VIB), Ghent University, B-9052 Gent, Belgium [3] Department of Plant Biotechnology and Genetics, Ghent University, B-9052 Gent, Belgium.

ABSTRACT
The prominent and evolutionarily ancient role of the plant hormone auxin is the regulation of cell expansion. Cell expansion requires ordered arrangement of the cytoskeleton but molecular mechanisms underlying its regulation by signalling molecules including auxin are unknown. Here we show in the model plant Arabidopsis thaliana that in elongating cells exogenous application of auxin or redistribution of endogenous auxin induces very rapid microtubule re-orientation from transverse to longitudinal, coherent with the inhibition of cell expansion. This fast auxin effect requires auxin binding protein 1 (ABP1) and involves a contribution of downstream signalling components such as ROP6 GTPase, ROP-interactive protein RIC1 and the microtubule-severing protein katanin. These components are required for rapid auxin- and ABP1-mediated re-orientation of microtubules to regulate cell elongation in roots and dark-grown hypocotyls as well as asymmetric growth during gravitropic responses.

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ABP1 is involved in MT rearrangement following gravistimulation(a) Rearrangement of MTs at the LS compared with the US of 90° reoriented roots of WT, SS12S, SS12K, abp1-5 (all expressing MAP4-GFP). Two different types of MTs orientation (90±30° or 0-60°/120-180°) were quantified. Student’s T-test was calculated for the category of transversal MTs in comparison to each 0’ time point and calculated for transversal MTs in the LS in comparison of the US at each time point (** p<0.001).(b-c) Auxin distribution simulated by DII-Venus at the LS compared with the US of 90° reoriented roots of SS12S and SS12K (all in DII-Venus background, enlarged pictures was visualized as the frames highlighted). Image stacks were taken every 10min, and in total 60 min (’). The ratio of the LS signal divided by the US one is shown in the chart (c). Student’s T-test was calculated for the signal ratio at each time point of SS12S/K compared with WT (** p<0.001). Signal intensity is represented by the color code as indicated. To be compared to WT data (Extended Data Fig. 1i-k).(d) The deviated angles of 90° gravistimulated-roots of WT, abp1-5, SS12S and SS12K seedlings were calculated for every 30min, in total 8h (Student’s T-test, *p<0.05, ** p<0.001).In all panels, error bars are s.e.m. Scale bars: 5 μm (a) and 30 μm (b).
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Figure 7: ABP1 is involved in MT rearrangement following gravistimulation(a) Rearrangement of MTs at the LS compared with the US of 90° reoriented roots of WT, SS12S, SS12K, abp1-5 (all expressing MAP4-GFP). Two different types of MTs orientation (90±30° or 0-60°/120-180°) were quantified. Student’s T-test was calculated for the category of transversal MTs in comparison to each 0’ time point and calculated for transversal MTs in the LS in comparison of the US at each time point (** p<0.001).(b-c) Auxin distribution simulated by DII-Venus at the LS compared with the US of 90° reoriented roots of SS12S and SS12K (all in DII-Venus background, enlarged pictures was visualized as the frames highlighted). Image stacks were taken every 10min, and in total 60 min (’). The ratio of the LS signal divided by the US one is shown in the chart (c). Student’s T-test was calculated for the signal ratio at each time point of SS12S/K compared with WT (** p<0.001). Signal intensity is represented by the color code as indicated. To be compared to WT data (Extended Data Fig. 1i-k).(d) The deviated angles of 90° gravistimulated-roots of WT, abp1-5, SS12S and SS12K seedlings were calculated for every 30min, in total 8h (Student’s T-test, *p<0.05, ** p<0.001).In all panels, error bars are s.e.m. Scale bars: 5 μm (a) and 30 μm (b).

Mentions: We also explored whether ABP1 function is required for the MT rearrangement and differential growth response in root gravitropism. Following 90° root reorientation, ABP1-inactivated lines showed much weaker MT rearrangement at the LS compared to WT (Extended Data Fig. 3a); however, gravity-induced asymmetric auxin distribution (monitored by DII:Venus) was also less pronounced in ABP1-inactivation lines (Extended Data Fig. 3b-c compared with Extended Data Fig.1i-k). In line with these observations, ABP1-deficient lines showed defects in gravitropic response (Extended Data Fig. 3d).


Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules.

Chen X, Grandont L, Li H, Hauschild R, Paque S, Abuzeineh A, Rakusová H, Benkova E, Perrot-Rechenmann C, Friml J - Nature (2014)

ABP1 is involved in MT rearrangement following gravistimulation(a) Rearrangement of MTs at the LS compared with the US of 90° reoriented roots of WT, SS12S, SS12K, abp1-5 (all expressing MAP4-GFP). Two different types of MTs orientation (90±30° or 0-60°/120-180°) were quantified. Student’s T-test was calculated for the category of transversal MTs in comparison to each 0’ time point and calculated for transversal MTs in the LS in comparison of the US at each time point (** p<0.001).(b-c) Auxin distribution simulated by DII-Venus at the LS compared with the US of 90° reoriented roots of SS12S and SS12K (all in DII-Venus background, enlarged pictures was visualized as the frames highlighted). Image stacks were taken every 10min, and in total 60 min (’). The ratio of the LS signal divided by the US one is shown in the chart (c). Student’s T-test was calculated for the signal ratio at each time point of SS12S/K compared with WT (** p<0.001). Signal intensity is represented by the color code as indicated. To be compared to WT data (Extended Data Fig. 1i-k).(d) The deviated angles of 90° gravistimulated-roots of WT, abp1-5, SS12S and SS12K seedlings were calculated for every 30min, in total 8h (Student’s T-test, *p<0.05, ** p<0.001).In all panels, error bars are s.e.m. Scale bars: 5 μm (a) and 30 μm (b).
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Figure 7: ABP1 is involved in MT rearrangement following gravistimulation(a) Rearrangement of MTs at the LS compared with the US of 90° reoriented roots of WT, SS12S, SS12K, abp1-5 (all expressing MAP4-GFP). Two different types of MTs orientation (90±30° or 0-60°/120-180°) were quantified. Student’s T-test was calculated for the category of transversal MTs in comparison to each 0’ time point and calculated for transversal MTs in the LS in comparison of the US at each time point (** p<0.001).(b-c) Auxin distribution simulated by DII-Venus at the LS compared with the US of 90° reoriented roots of SS12S and SS12K (all in DII-Venus background, enlarged pictures was visualized as the frames highlighted). Image stacks were taken every 10min, and in total 60 min (’). The ratio of the LS signal divided by the US one is shown in the chart (c). Student’s T-test was calculated for the signal ratio at each time point of SS12S/K compared with WT (** p<0.001). Signal intensity is represented by the color code as indicated. To be compared to WT data (Extended Data Fig. 1i-k).(d) The deviated angles of 90° gravistimulated-roots of WT, abp1-5, SS12S and SS12K seedlings were calculated for every 30min, in total 8h (Student’s T-test, *p<0.05, ** p<0.001).In all panels, error bars are s.e.m. Scale bars: 5 μm (a) and 30 μm (b).
Mentions: We also explored whether ABP1 function is required for the MT rearrangement and differential growth response in root gravitropism. Following 90° root reorientation, ABP1-inactivated lines showed much weaker MT rearrangement at the LS compared to WT (Extended Data Fig. 3a); however, gravity-induced asymmetric auxin distribution (monitored by DII:Venus) was also less pronounced in ABP1-inactivation lines (Extended Data Fig. 3b-c compared with Extended Data Fig.1i-k). In line with these observations, ABP1-deficient lines showed defects in gravitropic response (Extended Data Fig. 3d).

Bottom Line: Here we show in the model plant Arabidopsis thaliana that in elongating cells exogenous application of auxin or redistribution of endogenous auxin induces very rapid microtubule re-orientation from transverse to longitudinal, coherent with the inhibition of cell expansion.This fast auxin effect requires auxin binding protein 1 (ABP1) and involves a contribution of downstream signalling components such as ROP6 GTPase, ROP-interactive protein RIC1 and the microtubule-severing protein katanin.These components are required for rapid auxin- and ABP1-mediated re-orientation of microtubules to regulate cell elongation in roots and dark-grown hypocotyls as well as asymmetric growth during gravitropic responses.

View Article: PubMed Central - PubMed

Affiliation: 1] Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria [2] Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie (VIB), Ghent University, B-9052 Gent, Belgium [3] Department of Plant Biotechnology and Genetics, Ghent University, B-9052 Gent, Belgium.

ABSTRACT
The prominent and evolutionarily ancient role of the plant hormone auxin is the regulation of cell expansion. Cell expansion requires ordered arrangement of the cytoskeleton but molecular mechanisms underlying its regulation by signalling molecules including auxin are unknown. Here we show in the model plant Arabidopsis thaliana that in elongating cells exogenous application of auxin or redistribution of endogenous auxin induces very rapid microtubule re-orientation from transverse to longitudinal, coherent with the inhibition of cell expansion. This fast auxin effect requires auxin binding protein 1 (ABP1) and involves a contribution of downstream signalling components such as ROP6 GTPase, ROP-interactive protein RIC1 and the microtubule-severing protein katanin. These components are required for rapid auxin- and ABP1-mediated re-orientation of microtubules to regulate cell elongation in roots and dark-grown hypocotyls as well as asymmetric growth during gravitropic responses.

Show MeSH