Brassinosteroid-regulated GSK3/Shaggy-like Kinases Phosphorylate Mitogen-activated Protein (MAP) Kinase Kinases, Which Control Stomata Development in Arabidopsis thaliana

Khan, Mamoona; Rozhon, Wilfried; Bigeard, Jean; Pflieger, Delphine; Husar, Sigrid; Pitzschke, Andrea; Teige, Markus; Jonak, Claudia; Hirt, Heribert; Poppenberger, Brigitte

doi:10.1074/jbc.m112.384453

Cited by 156 publications

(153 citation statements)

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“…Recently, it was demonstrated that BIN2 integrates BR signaling and stomatal development in Arabidopsis (Gudesblat et al, 2012;Kim et al, 2012;Khan et al, 2013). Stomata formed by a pair of guard cells are essential for gas exchange and evaporation of water during photosynthesis and respiration throughout plant life.…”

Section: Introductionmentioning

confidence: 99%

Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12

Youn

Kim

et al. 2013

Molecules and Cells

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Plant GSK3-like kinases are key regulators that modulate a broad range of physiological processes such as cell growth, stomatal and flower development, responses for abiotic and biotic stress, and carbohydrate metabolism. Arabidopsis Shaggy/GSK3-like kinases (AtSK) consist of ten members that are classified into four subfamilies (I~IV). Only one of these Arabidopsis GSK3s, BIN2 (also named AtSK21), has been characterized by biochemical and genetic studies. BIN2 acts as a negative regulator in brassinosteroid (BR) signaling that controls cell growth and differentiation. Recent studies suggest that at least seven AtSKs are involved in BR signaling. However, specificities for the substrates and the functional differences of each member of the family remain to be determined. Here we report structural characteristics and distinct function of AtSK12 compared with BIN2. AtSK12 has a longer N-terminal extension, which is absent in BIN2. Transgenic plants overexpressing the AtSK12 mutant carrying deletion of Nterminal region display more severe dwarf phenotypes than those of the wild-type AtSK12. Microscopic analysis reveals that N-terminal-deleted AtSK12 accumulates in the nucleus. This implies that structural difference in the Nterminal region of AtSK members contributes to their subcellular localization. In contrast to BIN2, overexpression of AtSK12 does not cause a stomatal cluster. Furthermore, we show that YODA MAPKKK, which controls stomatal development, interacts with BIN2 but not with AtSK12. Our results suggest that AtSK12 mediates BR-regulated cell growth but not stomatal development while BIN2 regulates both processes. Our study provides evidence that different GSK3 members can have overlapping but non-identical functions.

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Section: Introductionmentioning

confidence: 99%

Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12

Youn

Kim

et al. 2013

Molecules and Cells

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“…In vitro kinase assays have shown that BIN2 also phosphorylates both MKK4 and MKK5 (Khan et al, 2013). In addition, BIN2 phosphorylation of MKK4 represses its activity against MPK6 in vitro ( Khan et al, 2013; Fig.…”

Section: Bin2 Phosphorylates Several Proteins In Stomatal Signaling Cmentioning

confidence: 99%

“…In addition, BIN2 phosphorylation of MKK4 represses its activity against MPK6 in vitro ( Khan et al, 2013; Fig. 1A).…”

Section: Bin2 Phosphorylates Several Proteins In Stomatal Signaling Cmentioning

confidence: 99%

“…1A). BIN2 phosphorylates two residues of MKK4 (Khan et al, 2013): Ser-230 and Thr-234. Since mutations in Thr-234 abolished the activity of MKK4 against MPK6 in vitro, Khan et al (2013) proposed that Thr-234 may be the main phosphorylation site of MKK4 by BIN2.…”

Section: Bin2 Phosphorylates Several Proteins In Stomatal Signaling Cmentioning

confidence: 99%

“…BIN2 phosphorylates two residues of MKK4 (Khan et al, 2013): Ser-230 and Thr-234. Since mutations in Thr-234 abolished the activity of MKK4 against MPK6 in vitro, Khan et al (2013) proposed that Thr-234 may be the main phosphorylation site of MKK4 by BIN2. Moreover, the overexpression of a mutant version of MKK4 in Thr-234, by replacing Thr with Ala to prevent phosphorylation, conferred a cotyledon epidermis composed almost entirely of stomata (Khan et al, 2013).…”

Section: Bin2 Phosphorylates Several Proteins In Stomatal Signaling Cmentioning

confidence: 99%

See 2 more Smart Citations

What Causes Opposing Actions of Brassinosteroids on Stomatal Development?

Serna

2013

Plant Physiol.

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Stomatal Patterning

Bringmann

Bergmann

2013

Encyclopedia of Life Sciences

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Stomatal development is a model for understanding the integration of multiple inputs into a simple cell fate choice. Intense research during the past decade has revealed mechanisms that govern stomatal development including inter‐ and intracellular signalling, transcriptional regulation, cell polarisation and asymmetric cell divisions. Recent discoveries in Arabidopsis include conserved families of transcription factors that drive differentiation and morphogenesis in the stomatal lineage. Specific proteins and pathways that mediate the transduction of signals, and thereby contribute to fate decisions such as secreted protein ligands, receptor kinases, mitogen activated protein kinase kinases and light and hormones have also recently been described. Studies in Arabidopsis and maize revealed novel proteins polarised within dividing stomatal lineage precursors. Together, these discoveries set the foundation to untangle mechanisms that lead to pattern and cell fate acquisition in plant systems. Key Concepts: Stomata are cellular pores that regulate gas exchange in plant leaves. Stomatal density and distribution is modulated by the environment and responds to changes in light, CO 2 and humidity. Stomatal development provides a framework for the understanding of cell fate, cell–cell signalling and cell polarity in plants. Progression through the stages of stomatal development in Arabidopsis requires a balance of fate promoting transcription factors, and fate and division repressing cell–cell signalling. Based on genetic studies, plants and animals display considerable conservation in the molecules and mechanisms used for developmental fates, but plant‐specific modules are used to generate physically asymmetric cell divisions that characterise early stomatal development.

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Brassinosteroid-regulated GSK3/Shaggy-like Kinases Phosphorylate Mitogen-activated Protein (MAP) Kinase Kinases, Which Control Stomata Development in Arabidopsis thaliana

Cited by 156 publications

References 55 publications

Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12

Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12

What Causes Opposing Actions of Brassinosteroids on Stomatal Development?

Stomatal Patterning

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