Changing proton concentrations at the surfaces of gravistimulated Phleum roots

Zieschang, Hanna; Köhler, Kurt; Sievers, Andreas

doi:10.1007/bf00224794

Cited by 37 publications

(33 citation statements)

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“…AGR1 activity could be directly regulated by gravity signals, promoting a differential flow of auxin on opposite flanks of a gravistimulated root (26). It is worth noting that fast changes in proton fluxes have been detected in proximity of the distal elongation zone in response to gravistimulation (27)(28)(29), indicating that this region can quickly respond to changes in root-tip orientation within the gravity field.…”

Section: Discussionmentioning

confidence: 99%

The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier

Chen

Hilson

Sedbrook

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

439

354

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Auxins are plant hormones that mediate many aspects of plant growth and development. In higher plants, auxins are polarly transported from sites of synthesis in the shoot apex to their sites of action in the basal regions of shoots and in roots. Polar auxin transport is an important aspect of auxin functions and is mediated by cellular inf lux and eff lux carriers. Little is known about the molecular identity of its regulatory component, the eff lux carrier [Estelle, M. (1996) Current Biol. 6, 1589-1591]. Here we show that mutations in the Arabidopsis thaliana AGRAVITROPIC 1 (AGR1) gene involved in root gravitropism confer increased root-growth sensitivity to auxin and decreased sensitivity to ethylene and an auxin transport inhibitor, and cause retention of exogenously added auxin in root tip cells. We used positional cloning to show that AGR1 encodes a putative transmembrane protein whose amino acid sequence shares homologies with bacterial transporters. When expressed in Saccharomyces cerevisiae, AGR1 promotes an increased eff lux of radiolabeled IAA from the cells and confers increased resistance to f luoro-IAA, a toxic IAA-derived compound. AGR1 transcripts were localized to the root distal elongation zone, a region undergoing a curvature response upon gravistimulation. We have identified several AGR1-related genes in Arabidopsis, suggesting a global role of this gene family in the control of auxin-regulated growth and developmental processes.Plant roots typically grow downward, at a defined angle from the gravity vector. They respond to deviations from the defined growth angle (gravistimulation) by developing a curvature at the distal and central elongation zones, which eventually allows their tip to resume a normal growth pattern. The gravitropic response involves perception of the gravistimulus by the root cap columella cells, transduction of that physical information into physiological signals, transmission of the signals to the distal and central elongation zones, and curvature response (1). Physiological evidence suggests that auxin and, possibly, apoplastic Ca 2ϩ constitute the physiological signals that are transmitted to the root distal and central elongation zones and are responsible for the curvature response (1).Basipetal transmission of auxin is mediated by polar auxin transport machinery, which involve influx and efflux carriers. The polarity of auxin transport probably is established by a basal localization of the efflux carrier in transporting cells (2). In this report, we demonstrate that the Arabidopsis thaliana AGR1 gene encodes a component of the auxin efflux carrier that mediates the root gravitropic response. MATERIALS AND METHODSPlant Stocks. The following alleles were analyzed and found to belong to the same complementation group: agr1-1, agr1-2, agr1-3 (Landsberg erecta; previously named as agr-1, agr-2, and agr-3, respectively) (3), agr1-4 (Wassilewskija; WS), agr1 , wav6 (Landsberg; agr1-52) (4), and eir1-1 (Columbia) (5). Manipulation of plant stocks was described previou...

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Section: Discussionmentioning

confidence: 99%

The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier

Chen

Hilson

Sedbrook

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

439

354

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“…Hence, gating of anion channels permeable for these anions would allow considerable efflux within a short time (Schmidt and Schroeder, 1994;Papernik and Kochian, 1997;Ryan et al, 1997). Even though there is agreement about the role of adequate cell wall pH in root elongation (Rayle and Cleland, 1992;Zieschang et al, 1993;Kutschera, 1994;Felle, 1998), a causal relation between the changes in pH profile observed and Al-induced inhibition of root growth remains a matter of debate (Ryan et al, 1992).…”

Section: Discussionmentioning

confidence: 99%

Genotypical Differences in Aluminum Resistance of Maize Are Expressed in the Distal Part of the Transition Zone. Is Reduced Basipetal Auxin Flow Involved in Inhibition of Root Elongation by Aluminum?

2000

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Short-term Al treatment (90 M Al at pH 4.5 for 1 h) of the distal transition zone (DTZ; 1-2 mm from the root tip), which does not contribute significantly to root elongation, inhibited root elongation in the main elongation zone (EZ; 2.5-5 mm from the root tip) to the same extent as treatment of the entire maize (Zea mays) root apex. Application of Al to the EZ had no effect on root elongation. Higher genotypical resistance to Al applied to the entire root apex, and specifically to the DTZ, was expressed by less inhibition of root elongation, Al accumulation, and Al-induced callose formation, primarily in the DTZ. A characteristic pH profile along the surface of the root apex with a maximum of pH 5.3 in the DTZ was demonstrated. Al application induced a substantial flattening of the pH profile moreso in the Al-sensitive than in the Al-resistant cultivar. Application of indole-3-acetic acid to the EZ but not to the meristematic zone significantly alleviated the inhibition of root elongation induced by the application of Al to the DTZ. Basipetal transport of exogenously applied [ 3 H]indole-3-acetic acid to the meristematic zone was significantly inhibited by Al application to the DTZ in the Al-sensitive maize cv Lixis. Our results provide evidence that the primary mechanisms of genotypical differences in Al resistance are located within the DTZ, and suggest a signaling pathway in the root apex mediating the Al signal between the DTZ and the EZ through basipetal auxin transport.The initial effect of Al toxicity is the inhibition of root elongation, a dramatic effect occurring within minutes after application. It is generally accepted that the root apex plays the major role in Al perception and response (for recent reviews, see Delhaize and Ryan, 1995;Horst, 1995; Kochian, 1995;Taylor, 1995;Rengel, 1996). This is well demonstrated by the fact that: (a) Al accumulation as an indicator of Al sensitivity occurs in the distal parts of the root apex (Delhaize et al., 1993a; Llugany et al., 1994;Sivaguru and Horst, 1998); (b) Al-resistance mechanisms, such as the release of Al-complexing organic compounds, are confined mainly to the root apex (Horst et al., 1982; Delhaize et al., 1993b; Pellet et al., 1995); and (c) callose formation, as a sensitive marker of Al sensitivity, is induced primarily in apical cells of the outer cortex (Wissemeier et al., 1987;Zhang et al., 1994;Wissemeier and Horst, 1995;Sivaguru and Horst, 1998). However, the question of the primary target of the Al effect remained open until recently. Ryan et al. (1993) showed that the root tip was most Al sensitive. Sivaguru and Horst (1998) presented evidence that the distal transition zone (DTZ) is the most Alsusceptible zone of the primary root of the Al-sensitive maize (Zea mays) cv Lixis. Subsequently, Sivaguru et al. (1999a) and Horst et al. (1999) showed that Al leads to alterations in the organization of microtubules and actin microfilaments, which were most severe in the DTZ. Although it is still a matter of debate whether Al affects the root ...

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“…Reduced Al uptake by the main MZ might be attributable to excretion of mucilage, which strongly binds Al (Archambault et al, 1996) and protects the root apex from Al injury (Horst et al, 1982). In the EZ, in contrast to the DTZ and TZ, an enhanced release of protons, leading to acidification of the apoplast (Monshausen et al, 1996) and thereby facilitating root growth (Weisenseel et al, 1992;Zieschang et al, 1993), could reduce the binding of Al to negative charges (Grauer and Horst, 1992;Kinraide, 1993).…”

Section: Discussionmentioning

confidence: 99%

The Distal Part of the Transition Zone Is the Most Aluminum-Sensitive Apical Root Zone of Maize1

1998

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Changing proton concentrations at the surfaces of gravistimulated Phleum roots

Cited by 37 publications

References 38 publications

The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier

The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier

Genotypical Differences in Aluminum Resistance of Maize Are Expressed in the Distal Part of the Transition Zone. Is Reduced Basipetal Auxin Flow Involved in Inhibition of Root Elongation by Aluminum?

The Distal Part of the Transition Zone Is the Most Aluminum-Sensitive Apical Root Zone of Maize1

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