Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor

Jaillais, Yvon; Hothorn, Michael; Belkhadir, Youssef; Dabi, Tsegaye; Nimchuk, Zachary L.; Meyerowitz, Elliot M.; Chory, Joanne

doi:10.1101/gad.2001911

Cited by 247 publications

(368 citation statements)

References 28 publications

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“…The irt1-1, irt1-1/35S::IRT1, irt1-1/35S::IRT1 K154RK179R , dominant negative clathrin hub DN-HUB1, RabF2a-mCherry, 2xFYVE HRS -mCherry, 2xFYVE HRS , BRI1-mCitrine, VHAa1-GFP, and VTI112-YFP lines were described in previous studies (2,15,18,19,34,37,53,54). The fyve1-1 insertion mutant (pst18264, Nossen ecotype) was isolated from the RIKEN collection.…”

Section: Methodsmentioning

confidence: 99%

Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis

Barberon

Dubeaux

Kolb

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

222

246

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In plants, the controlled absorption of soil nutrients by root epidermal cells is critical for growth and development. IRON-REGULATED TRANSPORTER 1 (IRT1) is the main root transporter taking up iron from the soil and is also the main entry route in plants for potentially toxic metals such as manganese, zinc, cobalt, and cadmium. Previous work demonstrated that the IRT1 protein localizes to early endosomes/trans-Golgi network (EE/TGN) and is constitutively endocytosed through a monoubiquitin-and clathrindependent mechanism. Here, we show that the availability of secondary non-iron metal substrates of IRT1 (Zn, Mn, and Co) controls the localization of IRT1 between the outer polar domain of the plasma membrane and EE/TGN in root epidermal cells. We also identify FYVE1, a phosphatidylinositol-3-phosphate-binding protein recruited to late endosomes, as an important regulator of IRT1-dependent metal transport and metal homeostasis in plants. FYVE1 controls IRT1 recycling to the plasma membrane and impacts the polar delivery of this transporter to the outer plasma membrane domain. This work establishes a functional link between the dynamics and the lateral polarity of IRT1 and the transport of its substrates, and identifies a molecular mechanism driving polar localization of a cell surface protein in plants.Arabidopsis | endocytosis | nutrition | radial transport | PI3P

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Section: Methodsmentioning

confidence: 99%

Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis

Barberon

Dubeaux

Kolb

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

222

246

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“…Donor vectors pDONR-P4P1R-UBQ10pro (Jaillais et al, 2011), pDONR221-AtPHYB (a gift of Kazu Nito), and pDONR-P2RP3-6xHis3xFlag tag were recombined with destination vector pK7m34GW. FPsc plants for transformation were grown on sterile agar plates, and young cotyledon explants were transformed with Agrobacterium tumefaciens GV3101 carrying the UBQ10pro::AtPHYB construct.…”

Section: Transformation Of B Rapa Fpscmentioning

confidence: 99%

Cotyledon-Generated Auxin Is Required for Shade-Induced Hypocotyl Growth in Brassica rapa

et al. 2014

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Plant architecture is optimized for the local light environment. In response to foliar shade or neighbor proximity (low red to far-red light), some plant species exhibit shade-avoiding phenotypes, including increased stem and hypocotyl growth, which increases the likelihood of outgrowing competitor plants. If shade persists, early flowering and the reallocation of growth resources to stem elongation ultimately affect the yield of harvestable tissues in crop species. Previous studies have shown that hypocotyl growth in low red to far-red shade is largely dependent on the photoreceptor phytochrome B and the phytohormone auxin. However, where shade is perceived in the plant and how auxin regulates growth spatially are less well understood. Using the oilseed and vegetable crop species Brassica rapa, we show that the perception of low red to far-red shade by the cotyledons triggers hypocotyl cell elongation and auxin target gene expression. Furthermore, we find that following shade perception, elevated auxin levels occur in a basipetal gradient away from the cotyledons and that this is coincident with a gradient of auxin target gene induction. These results show that cotyledon-generated auxin regulates hypocotyl elongation. In addition, we find in mature B. rapa plants that simulated shade does not affect seed oil composition but may affect seed yield. This suggests that in field settings where mutual shading between plants may occur, a balance between plant density and seed yield per plant needs to be achieved for maximum oil yield, while oil composition might remain constant.

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“…Subsequently, BRI1 can transphosphorylate BKI1, leading to the release of the kinase inhibitor into the cytosol (Jaillais et al, 2011b). The dissociation of BKI1 in turn may enable the recruitment of BAK1(SERK3) into the BRI1 receptor complex Kim and Wang, 2010;Jaillais et al, 2011aJaillais et al, , 2011b. Via sequential transphosphorylation events within the BRI1-BAK1 (SERK3) heterooligomers, BRI1 eventually gains full kinase activity and downstream BR signaling is initiated Kim and Wang, 2010;Clouse, 2011;Jaillais et al, 2011a).…”

mentioning

confidence: 99%

“…Binding of BRs to the extracellular LRR domain of BRI1 homodimers is thought to result in conformational changes, which trigger basal BRI1 kinase activity and autophosphorylation Kim and Wang, 2010;Jaillais et al, 2011a). Subsequently, BRI1 can transphosphorylate BKI1, leading to the release of the kinase inhibitor into the cytosol (Jaillais et al, 2011b). The dissociation of BKI1 in turn may enable the recruitment of BAK1(SERK3) into the BRI1 receptor complex Kim and Wang, 2010;Jaillais et al, 2011aJaillais et al, , 2011b.…”

mentioning

confidence: 99%

“…This inhibitory mechanism involves the BRI1 KINASE INHIBITOR1 (BKI1), which binds to the kinase domain of unliganded BRI1 receptors and thereby keeps the LRR-RLK inactive (Jaillais et al, 2011b). In vitro, BKI1 precludes BRI1 from associating with BRI1-ASSOCIATED KINASE1 (BAK1; also known as SOMATIC EMBRYO-GENESIS RECEPTOR-LIKE KINASE3 [SERK3]; Wang and Chory, 2006;Jaillais et al, 2011b), another LRR-RLK required for BR signal transduction Nam and Li, 2002;Gou et al, 2012). Binding of BRs to the extracellular LRR domain of BRI1 homodimers is thought to result in conformational changes, which trigger basal BRI1 kinase activity and autophosphorylation Kim and Wang, 2010;Jaillais et al, 2011a).…”

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confidence: 99%

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Visualization of BRI1 and BAK1(SERK3) Membrane Receptor Heterooligomers during Brassinosteroid Signaling

Bücherl¹,

Esse²,

Kruis³

et al. 2013

Plant Physiology

109

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The leucine-rich repeat receptor-like kinase BRASSINOSTEROID-INSENSITIVE1 (BRI1) is the main ligand-perceiving receptor for brassinosteroids (BRs) in Arabidopsis (Arabidopsis thaliana). Binding of BRs to the ectodomain of plasma membrane (PM)-located BRI1 receptors initiates an intracellular signal transduction cascade that influences various aspects of plant growth and development. Even though the major components of BR signaling have been revealed and the PM was identified as the main site of BRI1 signaling activity, the very first steps of signal transmission are still elusive. Recently, it was shown that the initiation of BR signal transduction requires the interaction of BRI1 with its SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) coreceptors. In addition, the resolved structure of the BRI1 ectodomain suggested that BRI1-ASSOCIATED KINASE1 [BAK1](SERK3) may constitute a component of the ligand-perceiving receptor complex. Therefore, we investigated the spatial correlation between BRI1 and BAK1(SERK3) in the natural habitat of both leucine-rich repeat receptor-like kinases using comparative colocalization analysis and fluorescence lifetime imaging microscopy. We show that activation of BR signaling by exogenous ligand application resulted in both elevated colocalization between BRI1 and BAK1(SERK3) and an about 50% increase of receptor heterooligomerization in the PM of live Arabidopsis root epidermal cells. However, large populations of BRI1 and BAK1(SERK3) colocalized independently of BRs. Moreover, we could visualize that approximately 7% of the BRI1 PM pool constitutively heterooligomerizes with BAK1(SERK3) in live root cells. We propose that only small populations of PMlocated BRI1 and BAK1(SERK3) receptors participate in active BR signaling and that the initiation of downstream signal transduction involves preassembled BRI1-BAK1(SERK3) heterooligomers.

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Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor

Cited by 247 publications

References 28 publications

Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis

Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis

Cotyledon-Generated Auxin Is Required for Shade-Induced Hypocotyl Growth in Brassica rapa

Visualization of BRI1 and BAK1(SERK3) Membrane Receptor Heterooligomers during Brassinosteroid Signaling

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