Cell signaling control by MAPK phospatases
Signals induced by environmental stress or during development have to be transmitted inside the cell to generate appropriate responses. In response to extracellular signals proteins are phosphorylated by reversible protein phosphorylation mechanism as a major principle of intracellular signaling, where protein phosphatases act as important regulators. The model plant Arabidopsis provides excellent possibilities to investigate regulation of stress-induced or developmental signalings on cellular and on the whole plant level.
The group studied Arabidopsis protein phosphatases of PP2C-type (AP2Cs) in regulation of signaling that is mediated by MAPKs (mitogen-activated protein kinases). They demonstrated that AP2Cs regulate activity of stress-induced MAPKs, which mediate pathogen and abiotic stress pathways as well as control of stomata development. Stomata are cells on plant epidermal surfaces that are specialized to regulate gas and water exchange with environment. Stomata developmental pathway involves MAPK signaling cascades and control by a PP2C-type MAPK phosphatase AP2C3. They showed that AP2C3 MAPK phosphatase modulates cell cycle and stomata differentiation, while AP2C1 MAPK phosphatase controls plant immunity and stress hormone production. Their findings revealed that gene expression profiles, different plant hormones and plant phenotypes are strongly affected by these MAPK phosphatases. They also studied how MAPK phosphatases channel signaling pathways towards specific responses under stress conditions and during cellular differentiation in stomata developmental pathway.
Arabidopsis MAPKs, such as MPK3, MPK4 and MPK6 are activated by phosphorylation of the conserved Thr and Tyr in their activation loop. This activation is induced in a minutes after exposure to stress, such as wounding of pathogen elicitors, but also during stomata development. Ser/Thr specific protein phosphatases from PP2C family AP2C1-4 dephosphorylate the phospho-Thr of the MAPK activation loop and thus inhibit their kinase activity. Inactivation of the MAPKs leads to the signal transduction „swich off“ ensuring its transient nature. Interestingly, stress and developmental signaling pathways are using the very same components, such as MPK3 and MPK6, to mediate signals to different responses, raising the question how the specificity is attained in these pathways. Our experiments performed on Arabidopsis plants demonstrated that AP2C1-4 gene expressions are stress-induced and tissue-specific, suggesting that AP2C protein phosphatases may coordinate inactivation of MPK3/MPK6/MPK4 in tissue/cell-specific manner or under stress conditions.
Studying protein phosphatase single and double mutant plants we have also succeeded to identify specific gene expression profiles induced by a specific MAPK pathway. They suggest that AP2C protein phosphatases may help to channel MAPK-mediated signals to specific targets. Our results are linking MAPK signaling to transcriptional reprogramming of plant cells and demonstrate importance of protein phosphatases in regulation of plant growth, development and survival under stress conditions.
Publications since 2006
Lee, Yang Ping; Giorgi, Federico M; Lohse, Marc; Kvederaviciute, Kotryna; Klages, Sven; Usadel, Björn; Meskiene, Irute; Reinhardt, Richard; Hincha, Dirk K (2013). Transcriptome sequencing and microarray design for functional genomics in the extremophile Arabidopsis relative Thellungiella salsuginea (Eutrema salsugineum). BMC GENOMICS;14:793. PMID: 24228715
Fuchs, Stefan; Grill, Erwin; Meskiene, Irute; Schweighofer, Alois (2012). Type 2C protein phosphatases in plants. FEBS J;280(2):681-93. PMID: 22726910
Umbrasaite, Julija; Schweighofer, Alois; Meskiene, Irute (2011). Substrate Analysis of Arabidopsis PP2C-Type Protein Phosphatases. Meth Mol Biol;779:149-61. PMID: 21837565
Umbrasaite, Julija; Schweighofer, Alois; Kazanaviciute, Vaiva; Magyar, Zoltan; Ayatollahi, Zahra; Unterwurzacher, Verena; Choopayak, Chonnanit; Boniecka, Justyna; Murray, James A H; Bogre, Laszlo; Meskiene, Irute (2010). MAPK phosphatase AP2C3 induces ectopic proliferation of epidermal cells leading to stomata development in Arabidopsis. PLOS ONE;5(12):e15357. PMID: 21203456
Schweighofer, Alois; Ayatollahi, Zahra; Meskiene, Irute (2009). Phosphatase activities analyzed by in vivo expressions. Meth Mol Biol;479:247-60. PMID: 19083183
Schweighofer, Alois; Meskiene, Irute (2008). Regulation of stress hormones jasmonates and ethylene by MAPK pathways in plants. MOL BIOSYST;4(8):799-803. PMID: 18633480
Schweighofer, Alois; Kazanaviciute, Vaiva; Scheikl, Elisabeth; Teige, Markus; Doczi, Robert; Hirt, Heribert; Schwanninger, Manfred; Kant, Merijn; Schuurink, Robert; Mauch, Felix; Buchala, Antony; Cardinale, Francesca; Meskiene, Irute (2007). The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. PLANT CELL;19(7):2213-24. PMID: 17630279
Michniewicz, Marta; Zago, Marcelo K; Abas, Lindy; Weijers, Dolf; Schweighofer, Alois; Meskiene, Irute; Heisler, Marcus G; Ohno, Carolyn; Zhang, Jing; Huang, Fang; Schwab, Rebecca; Weigel, Detlef; Meyerowitz, Elliot M; Luschnig, Christian; Offringa, Remko; Friml, Jirí (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. CELL;130(6):1044-56. PMID: 17889649