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Auxin influx carriers control vascular patterning and xylem differentiation in Arabidopsis thaliana.

Fàbregas N, Formosa-Jordan P, Confraria A, Siligato R, Alonso JM, Swarup R, Bennett MJ, Mähönen AP, Caño-Delgado AI, Ibañes M - PLoS Genet. (2015)

Bottom Line: Influx carriers increase cytoplasmic auxin signaling, and thereby differentiation.In addition to this cytoplasmic role of auxin, our computational simulations propose a role for extracellular auxin as an inhibitor of xylem differentiation.Altogether, our study shows that auxin influx carriers AUX1/LAX regulate vascular patterning and differentiation in plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Barcelona, Spain.

ABSTRACT
Auxin is an essential hormone for plant growth and development. Auxin influx carriers AUX1/LAX transport auxin into the cell, while auxin efflux carriers PIN pump it out of the cell. It is well established that efflux carriers play an important role in the shoot vascular patterning, yet the contribution of influx carriers to the shoot vasculature remains unknown. Here, we combined theoretical and experimental approaches to decipher the role of auxin influx carriers in the patterning and differentiation of vascular tissues in the Arabidopsis inflorescence stem. Our theoretical analysis predicts that influx carriers facilitate periodic patterning and modulate the periodicity of auxin maxima. In agreement, we observed fewer and more spaced vascular bundles in quadruple mutants plants of the auxin influx carriers aux1lax1lax2lax3. Furthermore, we show AUX1/LAX carriers promote xylem differentiation in both the shoot and the root tissues. Influx carriers increase cytoplasmic auxin signaling, and thereby differentiation. In addition to this cytoplasmic role of auxin, our computational simulations propose a role for extracellular auxin as an inhibitor of xylem differentiation. Altogether, our study shows that auxin influx carriers AUX1/LAX regulate vascular patterning and differentiation in plants.

No MeSH data available.


Related in: MedlinePlus

Theoretical and simulation results predict that auxin influx carriers facilitate periodic patterning and promote auxin maxima.(A) Snapshots of simulation results showing periodic distribution of auxin inside and outside cells for higher (left, I = 100 μM s-1) and lower (right, I = 0.001 μM s-1) influx carriers levels along a ring of vascular tissue composed of 60 cells surrounded by the apoplast. Cytosolic (blue) and apoplastic (green) auxin concentrations at time t = 17.5 are shown. The red circular line represents the ring of cells in the tissue. Insets depict the same results projected into a 2D plane. Space is represented in arbitrary units [AU]. Influx and efflux carriers distributions are described in S1 Text. (B) Simulation (boxplot) and theoretical estimation (κ, depicted by solid lines; see S1 Text) results of the inverse value of the number of cells between cytosolic auxin maxima at different influx carriers levels (I). Each boxplot depicts the results for 30 simulations with different initial auxin distributions (Materials and Methods). Simulations were done for rings of 60 cells. The bottom and the top of the boxes represent the first and third quartile, enclosing the 25%-75% data range, the red line within the box stands for the median, and the low and high whiskers enclose the 1.5×(25%-75%) data range. The theoretical estimation is performed through linear stability analysis for a ring of 60 and 1200 cells (black and blue lines, respectively). Theory and simulations show that influx impairment enlarges the periodicity of the pattern, increasing the distance between consecutive auxin maxima. (C) Phase diagram obtained from theoretical linear stability analysis on a ring of 60 cells on the parameters space of amount of influx carriers (I) and apoplastic diffusion coefficient (D). The solid line divides the space in two regions (Methods): in the H region (white, above the solid line) the homogeneous state is linearly stable and no periodic pattern can be formed from small perturbations of it. In the P region (colored, below the solid line) the homogeneous state is linearly unstable and a periodic pattern can arise. The dashed black line corresponds to an analytical approximation to the solid black line (S1 Text, Eq S34). The color scale shows the theoretical estimation of the inverse value of the average number of cells between cytosolic auxin maxima (κ). The horizontal dashed-dotted white line depicts the line along which simulations are presented in panels A and B. For low apoplastic diffusion D, periodic patterning can still occur at low influx parameter values I, while high influx values are necessary for patterning at higher apoplastic diffusion coefficients. Main parameter values: E = 105 μM s-1, D = 2 s-1, Dca = 15 s-1 and auxin threshold for transporters activation θI = θP = 10 μM. Other parameter values can be found in S1 Text.
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pgen.1005183.g001: Theoretical and simulation results predict that auxin influx carriers facilitate periodic patterning and promote auxin maxima.(A) Snapshots of simulation results showing periodic distribution of auxin inside and outside cells for higher (left, I = 100 μM s-1) and lower (right, I = 0.001 μM s-1) influx carriers levels along a ring of vascular tissue composed of 60 cells surrounded by the apoplast. Cytosolic (blue) and apoplastic (green) auxin concentrations at time t = 17.5 are shown. The red circular line represents the ring of cells in the tissue. Insets depict the same results projected into a 2D plane. Space is represented in arbitrary units [AU]. Influx and efflux carriers distributions are described in S1 Text. (B) Simulation (boxplot) and theoretical estimation (κ, depicted by solid lines; see S1 Text) results of the inverse value of the number of cells between cytosolic auxin maxima at different influx carriers levels (I). Each boxplot depicts the results for 30 simulations with different initial auxin distributions (Materials and Methods). Simulations were done for rings of 60 cells. The bottom and the top of the boxes represent the first and third quartile, enclosing the 25%-75% data range, the red line within the box stands for the median, and the low and high whiskers enclose the 1.5×(25%-75%) data range. The theoretical estimation is performed through linear stability analysis for a ring of 60 and 1200 cells (black and blue lines, respectively). Theory and simulations show that influx impairment enlarges the periodicity of the pattern, increasing the distance between consecutive auxin maxima. (C) Phase diagram obtained from theoretical linear stability analysis on a ring of 60 cells on the parameters space of amount of influx carriers (I) and apoplastic diffusion coefficient (D). The solid line divides the space in two regions (Methods): in the H region (white, above the solid line) the homogeneous state is linearly stable and no periodic pattern can be formed from small perturbations of it. In the P region (colored, below the solid line) the homogeneous state is linearly unstable and a periodic pattern can arise. The dashed black line corresponds to an analytical approximation to the solid black line (S1 Text, Eq S34). The color scale shows the theoretical estimation of the inverse value of the average number of cells between cytosolic auxin maxima (κ). The horizontal dashed-dotted white line depicts the line along which simulations are presented in panels A and B. For low apoplastic diffusion D, periodic patterning can still occur at low influx parameter values I, while high influx values are necessary for patterning at higher apoplastic diffusion coefficients. Main parameter values: E = 105 μM s-1, D = 2 s-1, Dca = 15 s-1 and auxin threshold for transporters activation θI = θP = 10 μM. Other parameter values can be found in S1 Text.

Mentions: Our analysis predicts that the amount of influx carriers can control the periodicity of the pattern, driving changes in the number of auxin maxima (Fig 1A and S1 Video). When the amount of influx carriers is decreased, less auxin maxima arise in a ring with a fixed number of cells (Fig 1A right panel). Hence, influx carriers promote auxin maxima to be closer together in terms of number of cells, up to a limit (Fig 1B and 1C). While pattern periodicity modulation was previously associated only to efflux carriers [3,4], our modeling results unveil a novel role for influx carriers in this process. Auxin entrance into the cells is essential for periodic pattern formation, by enabling the polar transport of auxin to take place. We confirmed that passive entrance into the cells, independently from influx carriers, can be enough to sustain periodic patterning, as expected (Fig 1C). Yet, we found that influx carriers become essential for patterning in high apoplastic diffusion conditions, in which passive entrance of auxin into the cell is not enough to enable the periodic patterning (Fig 1C and S1 Text). Therefore, our results show that influx carriers promote pattern formation as well.


Auxin influx carriers control vascular patterning and xylem differentiation in Arabidopsis thaliana.

Fàbregas N, Formosa-Jordan P, Confraria A, Siligato R, Alonso JM, Swarup R, Bennett MJ, Mähönen AP, Caño-Delgado AI, Ibañes M - PLoS Genet. (2015)

Theoretical and simulation results predict that auxin influx carriers facilitate periodic patterning and promote auxin maxima.(A) Snapshots of simulation results showing periodic distribution of auxin inside and outside cells for higher (left, I = 100 μM s-1) and lower (right, I = 0.001 μM s-1) influx carriers levels along a ring of vascular tissue composed of 60 cells surrounded by the apoplast. Cytosolic (blue) and apoplastic (green) auxin concentrations at time t = 17.5 are shown. The red circular line represents the ring of cells in the tissue. Insets depict the same results projected into a 2D plane. Space is represented in arbitrary units [AU]. Influx and efflux carriers distributions are described in S1 Text. (B) Simulation (boxplot) and theoretical estimation (κ, depicted by solid lines; see S1 Text) results of the inverse value of the number of cells between cytosolic auxin maxima at different influx carriers levels (I). Each boxplot depicts the results for 30 simulations with different initial auxin distributions (Materials and Methods). Simulations were done for rings of 60 cells. The bottom and the top of the boxes represent the first and third quartile, enclosing the 25%-75% data range, the red line within the box stands for the median, and the low and high whiskers enclose the 1.5×(25%-75%) data range. The theoretical estimation is performed through linear stability analysis for a ring of 60 and 1200 cells (black and blue lines, respectively). Theory and simulations show that influx impairment enlarges the periodicity of the pattern, increasing the distance between consecutive auxin maxima. (C) Phase diagram obtained from theoretical linear stability analysis on a ring of 60 cells on the parameters space of amount of influx carriers (I) and apoplastic diffusion coefficient (D). The solid line divides the space in two regions (Methods): in the H region (white, above the solid line) the homogeneous state is linearly stable and no periodic pattern can be formed from small perturbations of it. In the P region (colored, below the solid line) the homogeneous state is linearly unstable and a periodic pattern can arise. The dashed black line corresponds to an analytical approximation to the solid black line (S1 Text, Eq S34). The color scale shows the theoretical estimation of the inverse value of the average number of cells between cytosolic auxin maxima (κ). The horizontal dashed-dotted white line depicts the line along which simulations are presented in panels A and B. For low apoplastic diffusion D, periodic patterning can still occur at low influx parameter values I, while high influx values are necessary for patterning at higher apoplastic diffusion coefficients. Main parameter values: E = 105 μM s-1, D = 2 s-1, Dca = 15 s-1 and auxin threshold for transporters activation θI = θP = 10 μM. Other parameter values can be found in S1 Text.
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Related In: Results  -  Collection

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pgen.1005183.g001: Theoretical and simulation results predict that auxin influx carriers facilitate periodic patterning and promote auxin maxima.(A) Snapshots of simulation results showing periodic distribution of auxin inside and outside cells for higher (left, I = 100 μM s-1) and lower (right, I = 0.001 μM s-1) influx carriers levels along a ring of vascular tissue composed of 60 cells surrounded by the apoplast. Cytosolic (blue) and apoplastic (green) auxin concentrations at time t = 17.5 are shown. The red circular line represents the ring of cells in the tissue. Insets depict the same results projected into a 2D plane. Space is represented in arbitrary units [AU]. Influx and efflux carriers distributions are described in S1 Text. (B) Simulation (boxplot) and theoretical estimation (κ, depicted by solid lines; see S1 Text) results of the inverse value of the number of cells between cytosolic auxin maxima at different influx carriers levels (I). Each boxplot depicts the results for 30 simulations with different initial auxin distributions (Materials and Methods). Simulations were done for rings of 60 cells. The bottom and the top of the boxes represent the first and third quartile, enclosing the 25%-75% data range, the red line within the box stands for the median, and the low and high whiskers enclose the 1.5×(25%-75%) data range. The theoretical estimation is performed through linear stability analysis for a ring of 60 and 1200 cells (black and blue lines, respectively). Theory and simulations show that influx impairment enlarges the periodicity of the pattern, increasing the distance between consecutive auxin maxima. (C) Phase diagram obtained from theoretical linear stability analysis on a ring of 60 cells on the parameters space of amount of influx carriers (I) and apoplastic diffusion coefficient (D). The solid line divides the space in two regions (Methods): in the H region (white, above the solid line) the homogeneous state is linearly stable and no periodic pattern can be formed from small perturbations of it. In the P region (colored, below the solid line) the homogeneous state is linearly unstable and a periodic pattern can arise. The dashed black line corresponds to an analytical approximation to the solid black line (S1 Text, Eq S34). The color scale shows the theoretical estimation of the inverse value of the average number of cells between cytosolic auxin maxima (κ). The horizontal dashed-dotted white line depicts the line along which simulations are presented in panels A and B. For low apoplastic diffusion D, periodic patterning can still occur at low influx parameter values I, while high influx values are necessary for patterning at higher apoplastic diffusion coefficients. Main parameter values: E = 105 μM s-1, D = 2 s-1, Dca = 15 s-1 and auxin threshold for transporters activation θI = θP = 10 μM. Other parameter values can be found in S1 Text.
Mentions: Our analysis predicts that the amount of influx carriers can control the periodicity of the pattern, driving changes in the number of auxin maxima (Fig 1A and S1 Video). When the amount of influx carriers is decreased, less auxin maxima arise in a ring with a fixed number of cells (Fig 1A right panel). Hence, influx carriers promote auxin maxima to be closer together in terms of number of cells, up to a limit (Fig 1B and 1C). While pattern periodicity modulation was previously associated only to efflux carriers [3,4], our modeling results unveil a novel role for influx carriers in this process. Auxin entrance into the cells is essential for periodic pattern formation, by enabling the polar transport of auxin to take place. We confirmed that passive entrance into the cells, independently from influx carriers, can be enough to sustain periodic patterning, as expected (Fig 1C). Yet, we found that influx carriers become essential for patterning in high apoplastic diffusion conditions, in which passive entrance of auxin into the cell is not enough to enable the periodic patterning (Fig 1C and S1 Text). Therefore, our results show that influx carriers promote pattern formation as well.

Bottom Line: Influx carriers increase cytoplasmic auxin signaling, and thereby differentiation.In addition to this cytoplasmic role of auxin, our computational simulations propose a role for extracellular auxin as an inhibitor of xylem differentiation.Altogether, our study shows that auxin influx carriers AUX1/LAX regulate vascular patterning and differentiation in plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Barcelona, Spain.

ABSTRACT
Auxin is an essential hormone for plant growth and development. Auxin influx carriers AUX1/LAX transport auxin into the cell, while auxin efflux carriers PIN pump it out of the cell. It is well established that efflux carriers play an important role in the shoot vascular patterning, yet the contribution of influx carriers to the shoot vasculature remains unknown. Here, we combined theoretical and experimental approaches to decipher the role of auxin influx carriers in the patterning and differentiation of vascular tissues in the Arabidopsis inflorescence stem. Our theoretical analysis predicts that influx carriers facilitate periodic patterning and modulate the periodicity of auxin maxima. In agreement, we observed fewer and more spaced vascular bundles in quadruple mutants plants of the auxin influx carriers aux1lax1lax2lax3. Furthermore, we show AUX1/LAX carriers promote xylem differentiation in both the shoot and the root tissues. Influx carriers increase cytoplasmic auxin signaling, and thereby differentiation. In addition to this cytoplasmic role of auxin, our computational simulations propose a role for extracellular auxin as an inhibitor of xylem differentiation. Altogether, our study shows that auxin influx carriers AUX1/LAX regulate vascular patterning and differentiation in plants.

No MeSH data available.


Related in: MedlinePlus