A Role for Inositol 1,4,5-Trisphosphate in Gravitropic Signaling and the Retention of Cold-Perceived Gravistimulation of Oat Shoot Pulvini

Perera, Imara Y.; Heilmann, Ingo; Chang, Soo Chul; Boss, Wendy F.; Kaufman, Peter B.

doi:10.1104/pp.125.3.1499

Cited by 135 publications

(130 citation statements)

References 41 publications

(38 reference statements)

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“…A rapid increase and oscillation of inositol 1,4,5-trisphosphate (IP 3 ) levels was found in maize (Zea mays) pulvini after a gravitropic stimulus, lending further support to the role of phospholipid signaling in early gravitropic events (Perera et al, 1999). Perera et al (2001) showed that although cold treatment prevented the gravitropic response, IP 3 concentrations still changed in response to the gravity stimulation. The authors proposed that the cold treatment interrupted the events between IP 3 signaling and the establishment of an auxin asymmetry (Perera et al, 2001).…”

Section: Discussionmentioning

confidence: 96%

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Mutations in the Gravity Persistence Signal Loci in Arabidopsis Disrupt the Perception and/or Signal Transduction of Gravitropic Stimuli

et al. 2002

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Gravity plays a fundamental role in plant growth and development, yet little is understood about the early events of gravitropism. To identify genes affected in the signal perception and/or transduction phase of the gravity response, a mutant screen was devised using cold treatment to delay the gravity response of inflorescence stems of Arabidopsis. Inflorescence stems of Arabidopsis show no response to gravistimulation at 4°C for up to 3 h. However, when gravistimulated at 4°C and then returned to vertical at room temperature (RT), stems bend in response to the previous, horizontal gravistimulation (H. Fukaki, H. Fujisawa, M. Tasaka [1996] Plant Physiology 110: 933-943). This indicates that gravity perception, but not the gravitropic response, occurs at 4°C. Recessive mutations were identified at three loci using this cold effect on gravitropism to screen for gravity persistence signal (gps) mutants. All three mutants had an altered response after gravistimulation at 4°C, yet had phenotypically normal responses to stimulations at RT. gps1-1 did not bend in response to the 4°C gravity stimulus upon return to RT. gps2-1 responded to the 4°C stimulus but bent in the opposite direction. gps3-1 over-responded after return to RT, continuing to bend to an angle greater than wild-type plants. At 4°C, starch-containing statoliths sedimented normally in both wild-type and the gps mutants, but auxin transport was abolished at 4°C. These results are consistent with GPS loci affecting an aspect of the gravity signal perception/transduction pathway that occurs after statolith sedimentation, but before auxin transport.Gravity is a constant stimulus governing the orientation of plant growth. In response to changes in the gravity vector, plants reorient by differential growth. When placed horizontally, shoots and roots of a plant exhibit asymmetric growth resulting in upward or downward curvature, respectively. Gravitropism is only one part of a complex response network that integrates information from developmental and environmental stimuli (Ramussen, 1995). For simplicity, the response pathway has been separated into three sequential steps: gravity perception, signal transduction, and asymmetric growth response (for review, see Sack, 1991). The first step in gravity perception is the sedimentation of amyloplasts in shoots and roots (Sack, 1991;Kiss, 2000;Weise et al., 2000).Later aspects of the gravity response are driven by the asymmetric distribution of auxin that is thought to induce the differential growth that is required for gravitropic curvature (for review, see Muday, 2001). What is much less clear are the mechanisms by which statolith sedimentation initiates the transduction of the gravitropic signal and directs the asymmetric distribution of auxin.Arabidopsis has emerged as a powerful genetic model and has been useful in the dissection of the molecular mechanisms of the gravity response (Tasaka et al., 1999;Chen et al., 2002). Arabidopsis mutants with gravitropic response defects specific to the inflorescence stem, ...

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Section: Discussionmentioning

confidence: 96%

“…Perera et al (2001) showed that although cold treatment prevented the gravitropic response, IP 3 concentrations still changed in response to the gravity stimulation. The authors proposed that the cold treatment interrupted the events between IP 3 signaling and the establishment of an auxin asymmetry (Perera et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

Mutations in the Gravity Persistence Signal Loci in Arabidopsis Disrupt the Perception and/or Signal Transduction of Gravitropic Stimuli

et al. 2002

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“…The fastest responses were measured for phospholipase C-mediated changes of IP 3 levels in the cereal pulvini of oat and maize. A transient 5-fold increase in IP 3 within 10 s of gravity stimulation in the lower half of the pulvinus was detected (Perera et al, 1999(Perera et al, , 2001. Within less than a minute of gravity stimulation, changes in the cytosolic pH in the columella cells of the Arabidopsis root cap were evident (Scott and Allen, 1999;Fasano et al, 2001).…”

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confidence: 97%

The Fast and Transient Transcriptional Network of Gravity and Mechanical Stimulation in the Arabidopsis Root Apex

et al. 2004

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Plant root growth is affected by both gravity and mechanical stimulation . A coordinated response to both stimuli requires specific and common elements. To delineate the transcriptional response mechanisms, we carried out whole-genome microarray analysis of Arabidopsis root apices after gravity stimulation (reorientation) and mechanical stimulation and monitored transcript levels of 22,744 genes in a time course during the first hour after either stimulus. Rapid, transient changes in the relative abundance of specific transcripts occurred in response to gravity or mechanical stimulation, and these transcript level changes reveal clusters of coordinated events. Transcriptional regulation occurs in the root apices within less than 2 min after either stimulus. We identified genes responding specifically to each stimulus as well as transcripts regulated in both signal transduction pathways. Several unknown genes were specifically induced only during gravitropic stimulation (gravity induced genes). We also analyzed the network of transcriptional regulation during the early stages of gravitropism and mechanical stimulation.Plants adapt their growth in response to environmental cues. Gravity is a constant force that guides the direction of plant growth. Mechanical stimuli such as wind, rain, and obstacles in the soil trigger changes in growth patterns (Braam and Davis, 1990;. Gravitropic and mechanical stimulation in the root are interactive processes, mutually influencing differential growth (Mullen et al., 2000;Fasano et al., 2002;. The mechanisms of sensing and signal transduction for either stimulus are not well understood, but it has been shown that the transcript levels of specific genes are regulated early during signal transduction after either stimulus Braam and Davis, 1990).It is widely accepted that gravitropic stimulation by reorientation is perceived by sedimentation of starchcontaining plastids (statoliths) in the columella cells of the root tip (Kiss et al., 1989(Kiss et al., , 1996Juniper et al., 1966;Blancaflor et al., 1998). Columella cells show differences in their contribution toward gravity perception and in the velocity of sedimentation of their statoliths (Blancaflor et al., 1998). While complete sedimentation of the statoliths requires at least 5 min (Blancaflor et al., 1998;MacCleery and Kiss, 1999), the presentation time (duration of the stimulus that is required to establish a response) was estimated at only approximately 1 min for wild-type Arabidopsis root tips (Blancaflor et al., 1998). Statolith sedimentation is postulated to disrupt the actin-based cytoskeletal network and its links to plasma membrane receptors in some regions of the cell cortex (Yoder et al., 2001). Other groups hypothesized that statoliths are directly connected to the cytoskeleton, activating membrane proteins anchored to the filaments upon dislocation or activation of mechanosensitive ion channels (Evans et al., 1986;Pickard and Ding, 1993;Collings et al., 2001;Blancaflor, 2002).The transduction of the physical alt...

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“…Our previous pharmacological study using RR (Toyota et al, 2008a) suggests the involvement of endomembrane Ca 2+ -permeable channels in the sustained [Ca 2+ ] c increase. Intracellular inositol 1,4,5-trisphosphate (InsP 3 ) level is known to increase within 15 s of gravistimulation in oat (Avena sativa) shoot pulvini (Perera et al, 2001), suggesting the involvement of phospholipase C (PLC)-dependent signaling in the response to gravistimulation (Perera et al, 2006;Smith et al, 2013). Thus, InsP 3 -induced Ca 2+ release (Gilroy et al, 1990;Franklin-Tong et al, 1996;Knight et al, 1996) provides a potential mechanism for the sustained [Ca 2+ ] c increase that, once triggered, would be less sensitive to the gravity environment.…”

Section: Relationship Between the Amplitude Of The Sustained [Ca 2+ ]mentioning

confidence: 99%

Analyses of a Gravistimulation-Specific Ca2+ Signature in Arabidopsis using Parabolic Flights

et al. 2013

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Gravity is a critical environmental factor affecting the morphology and functions of organisms on the Earth. Plants sense changes in the gravity vector (gravistimulation) and regulate their growth direction accordingly. In Arabidopsis (Arabidopsis thaliana) seedlings, gravistimulation, achieved by rotating the specimens under the ambient 1g of the Earth, is known to induce a biphasic (transient and sustained) increase in cytoplasmic calcium concentration ([Ca 2+ ] c ). However, the [Ca 2+ ] c increase genuinely caused by gravistimulation has not been identified because gravistimulation is generally accompanied by rotation of specimens on the ground (1g), adding an additional mechanical signal to the treatment. Here, we demonstrate a gravistimulation-specific Ca 2+ response in Arabidopsis seedlings by separating rotation from gravistimulation by using the microgravity (less than 10 24 g) conditions provided by parabolic flights. Gravistimulation without rotating the specimen caused a sustained [Ca 2+ ] c increase, which corresponds closely to the second sustained [Ca 2+ ] c increase observed in ground experiments. The [Ca 2+ ] c increases were analyzed under a variety of gravity intensities (e.g. 0.5g, 1.5g, or 2g) combined with rapid switching between hypergravity and microgravity, demonstrating that Arabidopsis seedlings possess a very rapid gravity-sensing mechanism linearly transducing a wide range of gravitational changes (0.5g-2g) into Ca 2+ signals on a subsecond time scale.

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A Role for Inositol 1,4,5-Trisphosphate in Gravitropic Signaling and the Retention of Cold-Perceived Gravistimulation of Oat Shoot Pulvini

Cited by 135 publications

References 41 publications

Mutations in the Gravity Persistence Signal Loci in Arabidopsis Disrupt the Perception and/or Signal Transduction of Gravitropic Stimuli

Mutations in the Gravity Persistence Signal Loci in Arabidopsis Disrupt the Perception and/or Signal Transduction of Gravitropic Stimuli

The Fast and Transient Transcriptional Network of Gravity and Mechanical Stimulation in the Arabidopsis Root Apex

Analyses of a Gravistimulation-Specific Ca2+ Signature in Arabidopsis using Parabolic Flights

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