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

Abstract

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, ...

A Universal Role for Inositol 1,4,5-Trisphosphate-Mediated Signaling in Plant Gravitropism

“…Fukaki et al (1996a) showed that the memory or stored signal of the cold gravistimulus is retained for up to 60 min in Arabidopsis inflorescence stems. Wyatt et al (2002) have utilized this phenomenon to devise a creative screen for mutants impaired in some aspect of gravity signaling. We have shown previously that increases in InsP 3 can occur at 4°C in gravistimulated oat pulvini .…”

“…We have shown previously that increases in InsP 3 can occur at 4°C in gravistimulated oat pulvini . Furthermore, since the sedimentation of statoliths is not impaired by cold temperature (Wyatt et al, 2002), it is clear that gravity sensing and some of the early signaling can occur in the cold. In contrast, auxin transport is dramatically decreased in the cold (Morris, 1979;Wyatt et al, 2002), and cold temperature also affects cytoskeleton and membrane dynamics (Mizuno, 1992;Orvar et al, 2000;Sangwan et al, 2001).…”

Plant Gravitropism. Unraveling the Ups and Downs of a Complex Process

“…Another set of potential gravity signal transducers in shoots was identified in a clever genetic screen (Wyatt et al, 2002), taking advantage of the fact that Arabidopsis inflorescence stems can perceive a gravistimulus in the cold but cannot develop a curvature response under these conditions. Amazingly, Arabidopsis inflorescence stems that have been gravistimulated at 4°C can "remember" the signal for up to 1 h in the cold, such that a curvature response will be initiated if the stem is returned to room temperature during this time period (Fukaki et al, 1996).…”

“…The gps (gravity persistence signal) mutants were isolated for a defect in their ability to develop a curvature when returned to room temperature after they were gravistimulated at 4°C. The interesting properties of these mutants suggest that the GPS loci contribute to gravity perception or signal transduction at a step that follows amyloplast sedimentation but precedes lateral auxin transport (Wyatt et al, 2002). Molecular analysis of these mutations should provide important insights into the mechanisms that control gravity signal transduction in shoot statocytes.…”

Adaptive thermal control of stem gravitropism through alternative RNA splicing in Arabidopsis

“…At low temperatures, the gravitropism of inflorescence stems is declined in Arabidopsis, although gravity perception occurs normally. 5 When Arabidopsis plants are exposed to horizontal gravitropic stimulation under cold conditions and then returned to vertical orientation at 23 C, inflorescence stems bend in response to the previous horizontal gravistimulation, and statolith sedimentation occurs normally, 5,6 indicating that cold temperatures exert its effects after gravity perception.…”