Root-Gel Interactions and the Root Waving Behavior of Arabidopsis

Thompson, Matthew V.; Holbrook, N. Michele

doi:10.1104/pp.104.040881

Cited by 83 publications

(116 citation statements)

References 26 publications

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“…Root waving in wild-type plants is exaggerated when the plants are grown on back-tilted, stiff agar plates (Okada and Shimura, 1990;Rutherford and Masson, 1996;Rutherford et al, 1998;Thompson and Holbrook, 2004). The mdr1 phenotype shown here was similar when seedlings were grown on 0.8% agar or 1.5% agar plates (data not shown), indicating that it may be mechanistically distinct from conventional root waving.…”

Section: Spurious Curvature and Altered Auxin Distribution In Verticamentioning

confidence: 62%

Separating the Roles of Acropetal and Basipetal Auxin Transport on Gravitropism with Mutations in Two Arabidopsis Multidrug Resistance-Like ABC Transporter Genes

et al. 2007

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Two Arabidopsis thaliana ABC transporter genes linked to auxin transport by various previous results were studied in a reverse-genetic fashion. Mutations in Multidrug Resistance-Like1 (MDR1) reduced acropetal auxin transport in roots by 80% without affecting basipetal transport. Conversely, mutations in MDR4 blocked 50% of basipetal transport without affecting acropetal transport. Developmental and auxin distribution phenotypes associated with these altered auxin flows were studied with a high-resolution morphometric system and confocal microscopy, respectively. Vertically grown mdr1 roots produced positive and negative curvatures threefold greater than the wild type, possibly due to abnormal auxin distribution observed in the elongation zone. However, upon 90° reorientation, mdr1 gravitropism was inseparable from the wild type. Thus, acropetal auxin transport maintains straight growth but contributes surprisingly little to gravitropism. Conversely, vertically maintained mdr4 roots grew as straight as the wild type, but their gravitropism was enhanced. Upon reorientation, curvature in this mutant developed faster, was distributed more basally, and produced a greater total angle than the wild type. An amplified auxin asymmetry may explain the mdr4 hypertropism. Double mutant analysis indicated that the two auxin transport streams are more independent than interdependent. The hypothesis that flavanols regulate MDR-dependent auxin transport was supported by the epistatic relationship of mdr4 to the tt4 phenylpropanoid pathway mutation.

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Section: Spurious Curvature and Altered Auxin Distribution In Verticamentioning

confidence: 62%

Separating the Roles of Acropetal and Basipetal Auxin Transport on Gravitropism with Mutations in Two Arabidopsis Multidrug Resistance-Like ABC Transporter Genes

et al. 2007

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“…Even though CFR precedes root curvature (Mochizuki et al, 2005), suggesting the former might contribute to the latter, conditions have also been identified in which no CFR could be observed despite strong waving and skewing (Migliaccio and Piconese, 2001;Buer et al, 2003) or where CFR occurs in the absence of curving (Mullen et al, 1998;Sedbrook et al, 2002). It has been proposed that CFR illustrates a circumnutation-like process that contributes to waving and skewing on hard-agar surfaces (Rutherford and Masson, 1996;Simmons et al, 1996;Thompson and Holbrook, 2004). Alternatively, CFR and root bending may be mechanical consequences of impedance to root-tip movement by the agar surface (Thompson and Holbrook, 2004) or a secondary effect of the helical circumnutational movement of roots due to the necessity of discharging the energy accumulated by a flattening of the helix on the agar surface (Migliaccio and Piconese, 2001).…”

mentioning

confidence: 99%

“…If the surface is tilted backward, roots will form waves in addition to skewing. This pattern results from the root tip pressing on the surface when gravitropism directs downward growth Shimura, 1990, 1992;Rutherford and Masson, 1996;Simmons et al, 1996;Thompson and Holbrook, 2004). Root waving is usually accompanied by a reversible rotation of the tip about its axis, which manifests itself by a twisting of epidermal cell files (cell file rotation [CFR]) along the root (Okada and Shimura, 1990).…”

mentioning

confidence: 99%

Loss-of-Function Mutations of ROOT HAIR DEFECTIVE3 Suppress Root Waving, Skewing, and Epidermal Cell File Rotation in Arabidopsis

et al. 2005

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Wild-type Arabidopsis (Arabidopsis thaliana L. Heynh.) roots growing on a tilted surface of impenetrable hard-agar media adopt a wave-like pattern and tend to skew to the right of the gravity vector (when viewed from the back of the plate through the medium). Reversible root-tip rotation often accompanies the clockwise and counterclockwise curves that form each wave. These rotations are manifested by epidermal cell file rotation (CFR) along the root. Loss-of-function alleles of ROOT HAIR DEFECTIVE3 (RHD3), a gene previously implicated in the control of vesicle trafficking between the endoplasmic reticulum and the Golgi compartments, resulted in an almost complete suppression of epidermal CFR, root skewing, and waving on hard-agar surfaces. Several other root hair defective mutants (rhd2-1, rhd4-1, and rhd6-1) did not exhibit dramatic alterations in these root growth behaviors, suggesting that a generalized defect in root hair formation is not responsible for the surfacedependent phenotypes of rhd3. However, similar alterations in root growth behavior were observed in a variety of mutants characterized by defects in cell expansion (cob-1, cob-2, eto1-1, eto2-1, erh2-1, and erh3-1). The erh2-1 and rhd3-1 mutants differed from other anisotropic cell expansion mutants, though, by an inability to respond to low doses of the microtubule-binding drug propyzamide, which normally causes enhanced left-handed CFR and right skewing. We hypothesize that RHD3 may control epidermal CFR, root skewing, and waving on hard-agar surfaces by regulating the traffic of wall-or plasma membraneassociated determinants of anisotropic cell expansion.The primary roots of Arabidopsis (Arabidopsis thaliana L. Heynh.) seedlings display different growth behaviors depending on the conditions to which they are exposed. If grown within a homogenous environment (such as liquid or penetrable agar media), primary roots will grow downward in response to gravity (Blancaflor and Masson, 2003). When forced to grow on the surface of impenetrable hard-agar media, they will display more complex growth behaviors with characteristics dictated by the angle of the surface (Okada and Shimura, 1990). On surfaces tilted slightly forward, the roots of commonly used ecotypes will skew their growth to the right of the vertical when viewed through the agar medium, as per the established convention (Rutherford and Masson, 1996;Simmons et al., 1996). If the surface is tilted backward, roots will form waves in addition to skewing. This pattern results from the root tip pressing on the surface when gravitropism directs downward growth Shimura, 1990, 1992;Rutherford and Masson, 1996;Simmons et al., 1996;Thompson and Holbrook, 2004). Root waving is usually accompanied by a reversible rotation of the tip about its axis, which manifests itself by a twisting of epidermal cell files (cell file rotation [CFR]) along the root (Okada and Shimura, 1990). While curving to the right, roots tend to display left-handed CFR. By contrast, roots curving to the left display right-handed C...

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“…Arabidopsis root waving is essentially a flattenedspiral growth pattern on a firm agar medium, positioned at an angle of less than 90°with respect to the gravity vector (Okada and Shimura, 1990;Simmons et al, 1995;Mullen et al, 1998;Thompson and Holbrook, 2004). The wave pattern results mainly from the interaction of gravitropic and thigmotropic responses (Okada and Shimura, 1990;Thompson and Holbrook, 2004).…”

Section: Adaptive Significance For This Signal-integrated Root Growthmentioning

confidence: 99%

“…Root coiling on a hard surface is an estimate of the spiral-downward root pattern in the soil (Okada and Shimura, 1990;Garbers et al, 1996;Legué et al, 1997;Sack, 1997;Blancaflor et al, 1998;Luschnig et al, 1998;Rutherford et al, 1998;Marchant et al, 1999;Fasano et al, 2001;Rashotte et al, 2001;Gilroy, 2003a, 2003b;Piconese et al, 2003;Buer and Muday, 2004;Chen et al, 2009). Arabidopsis root waving is essentially a flattenedspiral growth pattern on a firm agar medium, positioned at an angle of less than 90°with respect to the gravity vector (Okada and Shimura, 1990;Simmons et al, 1995;Mullen et al, 1998;Thompson and Holbrook, 2004). The wave pattern results mainly from the interaction of gravitropic and thigmotropic responses (Okada and Shimura, 1990;Thompson and Holbrook, 2004).…”

Section: Adaptive Significance For This Signal-integrated Root Growthmentioning

confidence: 99%

Cytokinin Interplay with Ethylene, Auxin, and Glucose Signaling Controls Arabidopsis Seedling Root Directional Growth

2011

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(A.M.J.) Optimal root architecture is established by multiple intrinsic (e.g. hormones) and extrinsic (e.g. gravity and touch) signals and is established, in part, by directed root growth. We show that asymmetrical exposure of cytokinin (CK) at the root tip in Arabidopsis (Arabidopsis thaliana) promotes cell elongation that is potentiated by glucose in a hexokinase-influenced, G proteinindependent manner. This mode of CK signaling requires the CK receptor, ARABIDOPSIS HISTIDINE KINASE4 and, at a minimum, its cognate type B ARABIDOPSIS RESPONSE REGULATORS ARR1, ARR10, and ARR11 for full responsiveness, while type A response regulators act redundantly to attenuate this CK response. Ethylene signaling through the ethylene receptor ETHYLENE RESISTANT1 and its downstream signaling element ETHYLENE INSENSITIVE2 are required for CKinduced root cell elongation. Negative and positive feedback loops are reinforced by CK regulation of the expression of the genes encoding these elements in both the CK and ethylene signaling pathways. Auxin transport facilitated by PIN-FORMED2 as well as auxin signaling through control of the steady-state level of transcriptional repressors INDOLE-3-ACETIC ACID7 (IAA7), IAA14, and IAA17 via TRANSPORT INHIBITOR RESPONSE1/AUXIN SIGNALING F-BOX PROTEIN are involved in CK-induced root cell elongation. This action lies downstream of ethylene and CK induction. Intrinsic signaling in this response operates independently of the extrinsic signal touch, although actin filament organization, which is important in the touch response, may be important for this response, since latrunculin B can induce similar growth. This root growth response may have adaptive significance, since CK responsiveness is inversely related to root coiling and waving, two root behaviors known to be important for fitness.

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Root-Gel Interactions and the Root Waving Behavior of Arabidopsis

Cited by 83 publications

References 26 publications

Separating the Roles of Acropetal and Basipetal Auxin Transport on Gravitropism with Mutations in Two Arabidopsis Multidrug Resistance-Like ABC Transporter Genes

Separating the Roles of Acropetal and Basipetal Auxin Transport on Gravitropism with Mutations in Two Arabidopsis Multidrug Resistance-Like ABC Transporter Genes

Loss-of-Function Mutations of ROOT HAIR DEFECTIVE3 Suppress Root Waving, Skewing, and Epidermal Cell File Rotation in Arabidopsis

Cytokinin Interplay with Ethylene, Auxin, and Glucose Signaling Controls Arabidopsis Seedling Root Directional Growth

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