Gravity Signal Transduction in Primary Roots

Perrin, Robyn M.; Young, Li-Sen; Murthy, Uma; Harrison, Ben; Wang, Yan; Will, Jessica L.; Masson, Patrick

doi:10.1093/aob/mci227

Cited by 82 publications

(56 citation statements)

References 47 publications

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“…However, it is still interesting to investigate whether PIP5K2 also has impact on other auxin-related processes. Considering that other two important enzymes in the PI signaling pathway, phospholipase D (PLD) and inositol polyphosphate 5-phosphatase (5PTase) are both involved in auxin transport regulation, the root gravity response -another process regulated by auxin, specifically by polar auxin transport [57][58][59] was examined. As shown in Figure 4A, measurements of root curvature in response to gravity demonstrated that pip5k2 bent more slowly than WT, while transgenic lines with transformation rescue of PIP5K2 exhibited similar root curvature as WT, indicating a delayed root gravity response under PIP5K2 Fourday-old WT and pip5k2 seedlings were transferred to MS medium supplemented with IAA or NAA (0, 0.1 or 1 µM) for another 8 days, and lateral root density was measured and statistically analyzed using a heteroscedastic Student's t-test (*P < 0.01).…”

Section: Pip5k2 Has Delayed Root Gravity Response and Is Sensitive Tomentioning

confidence: 99%

Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins

et al. 2011

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Phosphatidylinositol monophosphate 5-kinase (PIP5K) catalyzes the synthesis of PI-4,5-bisphosphate (PtdIns(4,5) P 2 ) by phosphorylation of PI-4-phosphate at the 5 position of the inositol ring, and is involved in regulating multiple developmental processes and stress responses. We here report on the functional characterization of Arabidopsis PIP5K2, which is expressed during lateral root initiation and elongation, and whose expression is enhanced by exogenous auxin. The knockout mutant pip5k2 shows reduced lateral root formation, which could be recovered with exogenous auxin, and interestingly, delayed root gravity response that could not be recovered with exogenous auxin. Crossing with the DR5-GUS marker line and measurement of free IAA content confirmed the reduced auxin accumulation in pip5k2. In addition, analysis using the membrane-selective dye FM4-64 revealed the decelerated vesicle trafficking caused by PtdIns(4,5)P 2 reduction, which hence results in suppressed cycling of PIN proteins (PIN2 and 3), and delayed redistribution of PIN2 and auxin under gravistimulation in pip5k2 roots. On the contrary, PtdIns(4,5) P 2 significantly enhanced the vesicle trafficking and cycling of PIN proteins. These results demonstrate that PIP5K2 is involved in regulating lateral root formation and root gravity response, and reveal a critical role of PIP5K2/PtdIns(4,5)P 2 in root development through regulation of PIN proteins, providing direct evidence of crosstalk between the phosphatidylinositol signaling pathway and auxin response, and new insights into the control of polar auxin transport.

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Section: Pip5k2 Has Delayed Root Gravity Response and Is Sensitive Tomentioning

confidence: 99%

Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins

et al. 2011

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“…ARL2 and ARG1 function in the same genetic pathway as PIN3 in root gravitropism ARL2 and ARG1 encode similar J-domain proteins and may function in gravitropism by modulating the activity, localization or complex formation of other target proteins (Perrin et al, 2005). One candidate substrate for ARL2 and ARG1 in gravitropism is PIN3.…”

Section: Arl2mentioning

confidence: 99%

“…There is abundant evidence that amyloplasts are involved in gravity perception. However, to date there has been no definitive description of the mechanism that senses the position or movement of amyloplasts within the statocytes (Perrin et al, 2005). It has been proposed that sedimenting amyloplasts may trigger mechano-sensitive ion channels at the plasma membrane or ER, either directly, by sedimentation onto them (Sack, 1991;Zheng and Staehelin, 2001), or indirectly, by exerting pressure on the actin cytoskeleton (Sievers et al, 1989;Volkmann and Baluska, 1999) or disrupting its meshwork upon sedimentation (Yoder et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…It has been postulated that ARG1 functions in gravitropism by mediating changes in the activity and/or localization of proteins that are directly involved in gravity sensation and/or signal transduction . Candidates for these substrate proteins include PIN3 and other proteins that may mediate auxin transport through the root tip (Friml et al, 2002;Perrin et al, 2005), as well as proteins that may contribute to cytoplasmic alkalinization, such as H + -pyrophosphatases and members of the multi-subunit H + ATPase family (Li et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes

Harrison

Masson²

2007

The Plant Journal

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165

170

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SummaryALTERED RESPONSE TO GRAVITY1 (ARG1) and its paralog ARG1-LIKE2 (ARL2) are J-domain proteins that are required for normal root and hypocotyl gravitropism. In this paper, we show that both ARL2 and ARG1 function in a gravity signal transduction pathway with PIN3, an auxin efflux facilitator that is expressed in the statocytes. In gravi-stimulated roots, PIN3 relocalizes to the lower side of statocytes, a process that is thought to, in part, drive the asymmetrical redistribution of auxin toward the lower flank of the root. We show that ARL2 and ARG1 are required for PIN3 relocalization and asymmetrical distribution of auxin upon gravistimulation. ARL2 is expressed specifically in the root statocytes, where it localizes to the plasma membrane. Upon ectopic expression, ARL2 is also found at the cell plate of dividing cells during cytokinesis, an area of intense membrane dynamics. Mutations in ARL2 and ARG1 also result in auxin-related expansion of the root cap columella, consistent with a role for ARL2 and ARG1 in regulating auxin flux through the root tip. Together these data suggest that ARL2 and ARG1 functionally link gravity sensation in the statocytes to auxin redistribution through the root cap.

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“…Throughout their entire life cycle, plants use gravity to orient and coordinate their growth in order to maximize access to light, water, and nutrients. In directed growth in response to gravity (Perrin et al, 2005). This growth response is elicited by auxin concentration gradients that form across reoriented organs such that more of this hormone is present in the lower portion, as compared to the upper portion of the organs.…”

mentioning

confidence: 99%

An Endogenous Growth Pattern of Roots Is Revealed in Seedlings Grown in Microgravity

Millar

Johnson²,

Edelmann³

et al. 2011

Astrobiology

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In plants, sensitive and selective mechanisms have evolved to perceive and respond to light and gravity. We investigated the effects of microgravity on the growth and development of Arabidopsis thaliana (ecotype Landsberg) in a spaceflight experiment. These studies were performed with the Biological Research in Canisters (BRIC) hardware system in the middeck region of the space shuttle during mission STS-131 in April 2010. Seedlings were grown on nutrient agar in Petri dishes in BRIC hardware under dark conditions and then fixed in flight with paraformaldehyde, glutaraldehyde, or RNAlater. Although the long-term objective was to study the role of the actin cytoskeleton in gravity perception, in this article we focus on the analysis of morphology of seedlings that developed in microgravity. While previous spaceflight studies noted deleterious morphological effects due to the accumulation of ethylene gas, no such effects were observed in seedlings grown with the BRIC system. Seed germination was 89% in the spaceflight experiment and 91% in the ground control, and seedlings grew equally well in both conditions. However, roots of space-grown seedlings exhibited a significant difference (compared to the ground controls) in overall growth patterns in that they skewed to one direction. In addition, a greater number of adventitious roots formed from the axis of the hypocotyls in the flight-grown plants. Our hypothesis is that an endogenous response in plants causes the roots to skew and that this default growth response is largely masked by the normal 1 g conditions on Earth.

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Gravity Signal Transduction in Primary Roots

Abstract: These new discoveries illustrate the complexity of a highly redundant gravity-signalling process in roots, and help to elucidate the global mechanisms that govern auxin transport and morphogenetic regulation in roots.

Cited by 82 publications

References 47 publications

Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins

Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins

ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes

An Endogenous Growth Pattern of Roots Is Revealed in Seedlings Grown in Microgravity

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