Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway

Abstract

Plants must coordinately regulate biochemistry and anatomy to optimize photosynthesis and water use efficiency. The formation of stomata, epidermal pores facilitating gas exchange, is highly coordinated with other aspects of photosynthetic development. However, the signaling pathways controlling stomata development are not fully understood1,2, although Mitogen Activated Protein Kinase (MAPK) signaling is known to play key roles. Here we demonstrate that brassinosteroid (BR) regulates stomatal development by activating the MAPKKK, YODA. Genetic analyses indicate that receptor kinase-mediated BR signaling inhibits development through the GSK3-like kinase BIN2, and BIN2 acts upstream of YODA but downstream of the known ERECTA family of stomatal receptor kinases. Complementary in vitro and in vivo assays show that BIN2 phosphorylates YODA to inhibit YODA phosphorylation of its substrate MKK4, and activities of downstream MAPKs are reduced in BR-deficient mutants but increased by treatment with either BR or GSK3-kinase inhibitor. Our results indicate that BR inhibits stomatal development by alleviating GSK3-mediated inhibition of the MAPK module, providing two key links; that of a plant MAPKKK to its upstream regulators and BR to a specific developmental output.

Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF–TDR signalling

“…Recently it has been reported that BIN2 connects the BR signalling with Mitogen-Activated Protein Kinase (MAPK) pathway in the regulation of stomatal development 44,45 . BIN2 also functions as a hub between BR and auxin signalling pathways via phosphorylation of AUXIN RESPONSE FACTOR 2 (ARF2) by BIN2 (ref.…”

Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12

“…Recently, we demonstrated that BIN2 functions as a key regulator in stomatal development of Arabidopsis leaves (Kim et al, 2012). Plants overexpressing the BIN2 and bin2-1 mutants showed abnormal stomatal clusters and an increased number of stomata in the abaxial leaf epidermis.…”

“…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.…”

“…It was further demonstrated that BIN2 interacts with and inactivates YODA MAPKKK, leading to the acti-vation of SPEECHLESS. Bikinin, a specific inhibitor of GSK3-like kinases, strongly suppressed the stomatal cluster in both wild-type and the bin2-1 gain-of-function mutant, indicating that BR-regulated GSK3-like kinases mediate not only cell growth but also stomatal development (Kim et al, 2012). However, func-tional relevance of other AtSKs in stomatal development remains unknown.…”

What Causes Opposing Actions of Brassinosteroids on Stomatal Development?

“…Two works have revealed that BRs control stomatal production through regulating proteins that function in the stomatal pathway (Gudesblat et al, 2012a;Kim et al, 2012). However, while one of these studies showed that BRs repress stomatal development by alleviating the BIN2-mediated inhibition of YDA (Kim et al, 2012;Fig.…”