Abstract
Abscisic acid (ABA) is a phytohormone that regulates many physiological functions, such as plant growth, development and stress responses. The MAPK cascade plays an important role in ABA signal transduction. Several MAPK and MAPKK molecules are reported to function in ABA signaling; however, there have been few studies related to the identification of MAPKKK upstream of MAPKK in ABA signaling. In this study, we show that an Arabidopsis MAPKKK, MAPKKK18 functions in ABA signaling. The expression of MAPKKK18 was induced by ABA treatment. Yeast two-hybrid analysis revealed that MAPKKKK18 interacted with MKK3, which interacted with C-group MAPK, MPK1/2/7. Immunoprecipitated kinase assay showed that the 3xFlag-tagged MAPKKK18, expressed in Arabidopsis plants, was activated when treated with ABA. These results indicate the possibility that the MAPK cascade is composed of MAPKKK18, MKK3 and MPK1/2/7 in ABA signaling. The transgenic plants overexpressing MAPKKK18 (35S:MAPKKK18) and its kinase negative mutant (35S:MAPKKK18 KN) were generated, and their growth was monitored. Compared with the WT plant, 35S:MAPKKK18 and 35S:MAPKKK18 KN showed smaller and bigger phenotypes, respectively. Senescence of the rosette leaves was promoted in 35S:MAPKKK18, but suppressed in 35S:MAPKKK18 KN. Furthermore, ABA-induced leaf senescence was accelerated in 35S:MAPKKK18. These results suggest that MAPKKK18 controls the plant growth by adjusting the timing of senescence via its protein kinase activity in ABA dependent manners.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266. doi:10.1385/0-89603-391-0:259
Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226. doi:10.1042/BJ20080625
Dóczi R, Brader G, Pettkó-Szandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279. doi:10.1105/tpc.106.050039
Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166. doi:10.1199/tab.0166
Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708. doi:10.1101/gad.1953910
Hwa CM, Yang XC (2008) The AtMKK3 pathway mediates ABA and salt signaling in Arabidopsis. Acta Physiol Plant 30:277–286. doi:10.1007/s11738-007-0117-3
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24:655–665. doi:10.1046/j.1365-313x.2000.00913.x
Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, Cho D, Lee S, Giordo R, Sritubtim S, Leonhardt N, Ellis BE, Murata Y, Kwak JM (2009) MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci USA 106:20520–20525. doi:10.1073/pnas.0907205106
Khan M, Rozhon W, Poppenberger B (2014) The role of hormones in the aging of plants: a mini-review. Gerontology 60:49–55. doi:10.1159/000354334
Lee IC, Hong SW, Whang SS, Lim PO, Nam HG, Koo JC (2011) Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in arabidopsis leaves. Plant Cell Physiol 52:651–662. doi:10.1093/pcp/pcr026
Liu Y (2012) Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep 31:1–12. doi:10.1007/s00299-011-1130-y
MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308. doi:10.1016/S1360-1385(02)02302-6
Matsuoka D, Nanmori T, Sato K, Fukami Y, Kikkawa U, Yasuda T (2002) Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant J 29:637–647. doi:10.1046/j.0960-7412.2001.01246.x
Menges M, Dóczi R, Okrész L, Morandini P, Mizzi L, Soloviev M, Murray JA, Bögre L (2008) Comprehensive gene expression atlas for the Arabidopsis MAP kinase signalling pathways. New Phytol 179:643–662. doi:10.1111/j.1469-8137.2008.02552.x
Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327. doi:10.1371/journal.pbio.0040327
Munemasa S, Muroyama D, Nagahashi H, Nakamura Y, Mori IC, Murata Y (2013) Regulation of reactive oxygen species-mediated abscisic acid signaling in guard cells and drought tolerance by glutathione. Front Plant Sci 4:472. doi:10.3389/fpls.2013.00472
Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10:339–346. doi:10.1016/j.tplants.2005.05.009
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394. doi:10.1016/S0005-2728(89)80347-0
Sasayama D, Matsuoka D, Oka M, Shitamichi N, Furuya T, Azuma T, Itoh K, Nanmori T (2011) MAP3Kδ4, an Arabidopsis raf-like MAP3K, regulates plant growth and shoot branching. Plant Biotechnol 28:463–470. doi:10.5511/plantbiotechnology.11.1027a
Shitamici N, Matsuoka D, Sasayama D, Furuya T, Nanmori T (2013) Over-expression of MAP3Kδ4, an ABA-inducible raf-like MAP3K that confers salt tolerance in Arabidopsis. Plant Biotechnol 30:111–118. doi:10.5511/plantbiotechnology.13.0108a
Takahashi Y, Soyano T, Sasabe M, Machida Y (2004) A MAP kinase cascade that controls plant cytokinesis. J Biochem 136:127–132. doi:10.1093/jb/mvh118
Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292:2070–2072. doi:10.1126/science.1059046
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2(8):e718. doi:10.1371/journal.pone.0000718
Wise AA, Liu Z, Binns AN (2006) Three methods for the introduction of foreign DNA into Agrobacterium. Methods Mol Biol 343:43–53. doi:10.1385/1-59745-130-4:43
Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451. doi:10.1111/j.1365-313X.2008.03433.x
Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–795. doi:10.1038/nature06543
Zhang K, Xia X, Zhang Y, Gan SS (2012) An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J 69:667–678. doi:10.1111/j.1365-313X.2011.04821.x
Zhou C, Cai Z, Guo Y, Gan S (2009) An Arabidopsis mitogen-activated protein kinase cascade, MKK9–MPK6, plays a role in leaf senescence. Plant Physiol 150:167–177. doi:10.1104/pp.108.133439
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsuoka, D., Yasufuku, T., Furuya, T. et al. An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol Biol 87, 565–575 (2015). https://doi.org/10.1007/s11103-015-0295-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-015-0295-0