Control of gravimorphogenesis by auxin: accumulation pattern of CS-IAA1 mRNA in cucumber seedlings grown in space and on the ground

Kamada, Motoshi; Fujii, Nobuharu; Aizawa, Sachiko; Kamigaichi, Shigeki; Mukai, Chiaki; Shimazu, Toru; Takahashi, Hideyuki

doi:10.1007/s004250000321

Cited by 40 publications

(35 citation statements)

References 30 publications

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“…The Cholodny-Went hypothesis proposes that a gradient of auxin is generated as a result of a gravity signal, stimulating a gradient of growth rate changes in cells across the tissue (Lomax, 1997). This hypothesis has been supported by studies on auxin redistribution (Lomax, 1997) and by the observation that gravistimulation results in asymmetrically induced auxin-responsive genes (McClure and Guilfoyle, 1989;Li et al, 1991;Kamada et al, 2000;Rashotte et al, 2001). In the oat pulvinus, 24 h of gravistimulation results in asymmetrical changes in free IAA levels with a 2.5-fold increase in free IAA in the lower one-half compared with the upper one-half of the oat pulvinus (Brock et al, 1991;Kaufman et al, 1995).…”

supporting

confidence: 55%

Gravity-Stimulated Changes in Auxin and Invertase Gene Expression in Maize Pulvinal Cells

Long¹,

Zhao²,

Rashotte

et al. 2002

Plant Physiology

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(A.M.R., G.K.M.) Maize (Zea mays) stem gravitropism involves differential elongation of cells within a highly specialized region, the stem internodal pulvinus. In the present study, we investigated factors that control gravitropic responses in this system. In the graviresponding pulvinus, hexose sugars (d-Glc and d-Fru) accumulated asymmetrically across the pulvinus. This correlated well with an asymmetric increase in acid invertase activity across the pulvinus. Northern analyses revealed asymmetric induction of one maize acid invertase gene, Ivr2, consistent with transcriptional regulation by gravistimulation. Several lines of evidence indicated that auxin redistribution, as a result of polar auxin transport, is necessary for gravity-stimulated Ivr2 transcript accumulation and differential cell elongation across the maize pulvinus. First, the auxin transport inhibitor, N-1-naphthylphthalamic acid, inhibited gravistimulated curvature and Ivr2 transcript accumulation. Second, a transient gradient of free indole-3-acetic acid (IAA) across the pulvinus was apparent shortly after initiation of gravistimulation. This temporarily free IAA gradient appears to be important for differential cell elongation and Ivr2 transcript accumulation. This is based on the observation that N-1-naphthylphthalamic acid will not inhibit gravitropic responses when applied to pulvinus tissue after the free IAA gradient peak has occurred. Third, IAA alone can stimulate Ivr2 transcript accumulation in non-gravistimulated pulvini. The gravity-and IAA-stimulated increase in Ivr2 transcripts was sensitive to the protein synthesis inhibitor, cycloheximide. Based on these results, a two-phase model describing possible relationships between gravitropic curvature, IAA redistribution, and Ivr2 expression is presented.Maintaining plant organs with respect to the gravity vector is crucial for proper plant development. Plants use the gravity vector as a cue to orient shoots and roots, positioning leaves for maximum light and roots for maximum water and nutrient uptake (Chen et al., 1999). Plants are able to perceive a change in the direction of the gravity vector. Signal transduction pathway(s) transmit this information, resulting in a differential growth response that returns the plant back to its normal position relative to the gravity vector. Using a genetic approach, some of the early key components of gravitropism have been elucidated (Chen et al., 1999). However, the pathways and mechanisms involved in gravity perception and signal transduction are still not very well understood.Grass shoots have recently emerged as an excellent model system for studying gravitropism signaling events and responses. In grass shoots, gravitropism occurs at a specific region called the pulvinus. In maize (Zea mays), the focus of this study, the pulvinus is located at the base of the internode (Collings et al., 1998). Surrounding the vascular bundles within the maize pulvinus are several layers of bundle sheath cells. These cells contain starch-filled, sedimenta...

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supporting

confidence: 55%

Gravity-Stimulated Changes in Auxin and Invertase Gene Expression in Maize Pulvinal Cells

Long¹,

Zhao²,

Rashotte

et al. 2002

Plant Physiology

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“…It has been suggested that auxin is a factor that regulates peg formation (Witztum and Gersani, 1975;Takahashi and Scott, 1994;Kamada et al, 2000) as application of exogenous auxin induces peg formation on the convex side of the transition zone (Witztum and Gersani, 1975;Kamada et al, 2000). It has also been found that, in cucumber seedlings grown in a horizontal position, the levels of free indole-3-acetic acid (IAA) are more abundant in the concave side than in the convex side (Kamada et al, 2003).…”

Section: Introductionmentioning

confidence: 94%

Possible Involvement of CS-ACS1 and Ethylene in Auxin-induced Peg Formation of Cucumber Seedlings

et al. 2004

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Background and Aims Cucumber (Cucumis sativus) seedlings develop a peg on the concave side of the gravitropically bending transition zone between the hypocotyl and the root after seed germination. Peg initiation occurs in response to auxin when its levels in the concave side of the transition zone exceed a particular threshold through the graviresponse. Ethylene also plays an important role in peg formation, but its relationship to auxin in this event is not understood. Here, the role ethylene plays in auxin-induced peg formation is studied.Methods Peg formation of cucumber seedlings exposed to ethylene at different stages of growth or during exogenous auxin treatment was observed. In addition, ethylene evolution from the concave and convex sides of the transition zone was compared and their transcription of CS-ACS (1-aminocyclopropane-1-carboxylic acid synthase) genes was analysed by RT-PCR and in situ hybridization.Key Results Seedlings treated with ethylene after peg initiation produced an enlarged peg, whereas ethylene treatment before peg initiation inhibited peg formation. Ethylene also promoted the development of the peg in the auxin-treated seedlings. Furthermore, the concave side of the transition zone at peg initiation produced more ethylene and CS-ACS1 mRNA than the convex side.Conclusions Since CS-ACS1 is an auxin-inducible gene, the greater abundance of auxin in the concave side of the transition zone causes peg initiation and increases CS-ACS1-mediated ethylene biosynthesis, which then facilitates peg development.

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“…This gravity response of Mock 92.6 6 6.5 7.4 6 6.5 0.0 6 0.0 10 25 M TIBA 92.6 6 6.5 7.4 6 6.5 0.0 6 0.0 10 24 M TIBA 3.5 6 3.0* 96.5 6 3.0* 0.0 6 0.0 10 23 M TIBA 2.4 6 4.1* 88.4 6 4.8* 9.3 6 8.5* CsPIN1 localization occurred on the upper side of the transition zone and was consistent with the findings of spaceflight experiments . Gravistimulation is suspected to induce asymmetric auxin distribution in the transition zone and influence the location of peg formation Kamada et al, 2000Kamada et al, , 2003Saito et al, 2004Saito et al, , 2005. The application of TIBA, an inhibitor of auxin efflux, induces peg formation on the upper side of the transition zone of cucumber seedlings grown horizontally .…”

Section: Change In Cspin1 Accumulation In the Endodermis Of The Transmentioning

confidence: 99%

“…Both endogenous indole-3-acetic acid (IAA) concentration and auxin-inducible gene expression are significantly reduced on the peg-suppressed side (the upper side) of the transition zone Kamada et al, 2000). Application of exogenous auxin induces the development of a peg on the upper side of the transition zone in a horizontal position .…”

mentioning

confidence: 99%

Gravistimulation Changes the Accumulation Pattern of the CsPIN1 Auxin Efflux Facilitator in the Endodermis of the Transition Zone in Cucumber Seedlings

Watanabe

Fujii²,

Yanai³

et al. 2011

Plant Physiology

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Cucumber (Cucumis sativus) seedlings grown in a horizontal position develop a specialized protuberance (or peg) on the lower side of the transition zone between the hypocotyl and the root. This occurs by suppressing peg formation on the upper side via a decrease in auxin resulting from a gravitational response. However, the gravity-stimulated mechanism of inducing asymmetric auxin distribution in the transition zone is poorly understood. The gravity-sensing tissue responsible for regulating auxin distribution in the transition zone is thought to be the endodermal cell. To characterize the gravity-stimulated mechanism, the auxin efflux facilitator PIN-FORMED1 (CsPIN1) in the endodermis was identified and the localization of CsPIN1 proteins during the gravimorphogenesis of cucumber seedlings was examined. Immunohistochemical analysis revealed that the accumulation pattern of CsPIN1 protein in the endodermal cells of the transition zone of cucumber seedlings grown horizontally differed from that of plants grown vertically. Gravistimulation for 30 min prompted changes in the accumulation pattern of CsPIN1 protein in the endodermis as well as the asymmetric distribution of auxin in the transition zone. Furthermore, 2,3,5-triiodobenzoic acid inhibited the differential distribution of auxin as well as changes in the accumulation pattern of CsPIN1 in the endodermis of the transition zone during gravistimulation. These results suggest that the altered pattern of CsPIN1 accumulation in the endodermis in response to gravistimulation influences lateral auxin transport through the endodermis, resulting in asymmetric auxin distribution in the transition zone.

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Control of gravimorphogenesis by auxin: accumulation pattern of CS-IAA1 mRNA in cucumber seedlings grown in space and on the ground

Cited by 40 publications

References 30 publications

Gravity-Stimulated Changes in Auxin and Invertase Gene Expression in Maize Pulvinal Cells

Gravity-Stimulated Changes in Auxin and Invertase Gene Expression in Maize Pulvinal Cells

Possible Involvement of CS-ACS1 and Ethylene in Auxin-induced Peg Formation of Cucumber Seedlings

Gravistimulation Changes the Accumulation Pattern of the CsPIN1 Auxin Efflux Facilitator in the Endodermis of the Transition Zone in Cucumber Seedlings

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