摘要
促分裂原活化蛋白激酶(mitogen activated protein kinase, MAPK)级联途径是真核生物中广泛存在的信号转导途径。促分裂原活化蛋白激酶级联途径由MAPKKK-MAPKK-MAPK依次磷酸化传递信号。MAPK级联途径各激酶基因家族在不同植物物种中是保守的。目前,玉米基因组测序已经完成,在基因组水平上解析玉米MAPK家族的信息已经成为可能。MAPK是连接底物和上游信号的重要因子。以前的研究表明,MAPK级联途径参与植物的ABA信号转导。但是,关于ABA信号中特异的MAPK基因的研究仍然很有限。
本研究根据植物MAPK基因的保守性鉴定了玉米MAPK家族的基因。对玉米MAPK基因家族的分类、蛋白生化特性、基因结构、染色体分布、蛋白的系统进化以及基因在幼苗根、茎、叶中的表达模式进行了系统分析。在此基础之上,选取了ZmMPK4基因进行功能研究。ZmMPK4为双拷贝基因,和ZmMPK3是基因对,ZmMPK4基因对参与ABA信号转导。主要研究结果如下:
(1)利用网络数据库的BLAST和本地Stand-alone BLAST的方法,鉴定了19个玉米MAPK基因。19个MAPK基因的氨基酸长度在369到642之间,分子量在42.199 kDa到72.444 kDa之间,等电点在5.26到9.82之间。6号和8号染色体各有4个MAPK基因,5号和9号各3个,10号2个,1号、3号、4号各1个。与双子叶拟南芥和杨树比较,玉米MAPK基因和水稻MAPK基因的亲缘关系比较近。
(2)ZmMPK1和ZmMPK2的序列高度相似,数据库搜索表明,没有EST序列特异的和ZmMPK1匹配。RT-PCR分析表明,在玉米幼苗根、茎、叶中检测不到ZmMPK1的表达,说明ZmMPK1可能是一个假基因。其它18个基因在玉米幼苗根、茎、叶中都能检测到。除了ZmMPK12、ZmMPK18、ZmMPK19没有明显的组织特异性外,其它15个基因在玉米幼苗根、茎、叶中的分布均不同。
(3)PCR分析表明,ZmMPK4和文献报道的ZmMPK4(命名为ZmMPK4-2)的序列不完全一致。ZmMPK4-2是ZmMPK4的一个可变剪接产物。基因测序和玉米MAPK基因家族的分析表明,ZmMPK4是双拷贝基因,ZmMPK3和ZmMPK4是基因对。Southern实验验证了ZmMPK4的拷贝数。ZmMPK3和ZmMPK4的核苷酸相似度为92.1%,编码氨基酸的相似度为90.0%。ZmMPK3和ZmMPK4分别位于1号染色体短臂和9号染色体长臂。两个基因都能形成mRNA和蛋白质。
(4)序列分析表明,ZmMPK4的3号内含子是GC-AG型内含子。ZmMPK4-2是保留了ZmMPK4的3号内含子形成的可变剪接产物。ZmMPK4-2的组成型表达量非常低,主要在叶中表达。ZmMPK4也可以剪切3号内含子形成正常的ZmMPK4-1,且为ZmMPK4基因表达的主要方式。ZmMPK3的3号内含子为GT-AG型内含子。
(5)Northern杂交实验表明,ZmMPK3主要在生长5日的幼苗叶中表达,ZmMPK4主要在幼苗根中表达。ZmMPK3和ZmMPK4都受ABA(100?M)和NaCl(200mM)的诱导,但诱导时间和表达量不同。但是,Northern杂交不能区分ZmMPK4-1和ZmMPK4-2。利用RT-PCR的方法,进一步分析了ZmMPK4-1和ZmMPK4-2的特异表达,结果显示,ZmMPK4-2主要在叶中表达,即ZmMPK4在幼苗中的可变剪接主要在叶中进行。ZmMPK4的可变剪接受ABA或NaCl的调控。
(6)制备了ZmMPK3的抗体(Anti-ZmMPK3)。因为ZmMPK3和ZmMPK4的氨基酸序列高度相似,无法设计特异抗体。ZmMPK3和ZmMPK4的混合蛋白(约43kDa)在生长5d的玉米叶片中组成型表达,ABA(100?M)可以轻微诱导ZmMPK3和ZmMPK4混合蛋白的表达。免疫沉淀分析表明,ABA可以激活ZmMPK3和ZmMPK4混合蛋白的激酶活性(0.5h和1h)。用烟草叶片瞬时转化法分别检测ZmMPK3、ZmMPK4-1和ZmMPK4-2的活性,检测不到ZmMPK4-2的活性,而ZmMPK3或ZmMPK4-1的激酶活性都可以被ABA诱导。
(7)洋葱表皮表达分析表明,ZmMPK3或ZmMPK4-1的融合蛋白主要定位于细胞膜和细胞核,而ZmMPK4-2融合蛋白主要定位于细胞膜和细胞质。ZmMPK4-2中的30个氨基酸的插入可能影响ZmMPK4的细胞定位。
(8)过表达ZmMPK4-1可以促进拟南芥提前抽薹。在发育后期,转基因拟南芥的主茎上可以形成莲座叶,并可继续抽薹。在正常MS培养基上,过表达ZmMPK4-1的拟南芥和野生型拟南芥的萌发率没有明显差别(约为100%)。0.5?M的ABA可以抑制转基因和野生型拟南芥种子的萌发,但对转基因拟南芥的抑制明显强于野生型。正常生长条件下,ZmMPK4-1在转基因拟南芥中具有激酶活性。ABA(0.5?M)可以增强转基因拟南芥中ZmMPK4-1的激酶活性。过表达ZmMPK4-1可以诱导拟南芥AtACT1的组成型表达,可以增强AtACT2、ABI3、ABI5基因对ABA(0.5?M)的响应。
Mitogen-activated protein kinase (MAPK) cascades are universal signal transduction modules in eukaryotes. A MAPK cascade consists of MAPKKK-MAPKK-MAPK, that sequentially phosphorylate the corresponding downstream substrates. Each gene family of MAPKKK, MAPKK or MAPK is conserved in different plant species. The maize genome has been sequenced to date. It is possible to dissect the information of maize MAPK gene family based on the genomic sequence. MAPK links upstream components to downstream substrates. Previously, it has been reported that MAPK cascades participated in ABA signaling. However, the specific MAPK gene in ABA signaling is still sparse.
In this study, we identified MAPK genes in the maize genome based on the conservation of plant MAPKs. The classification, the protein properties, the gene structure, the chromosomal distribution, the evolutionary relationship and the expression pattern in maize roots, stems and leaves of maize MAPK genes have been analyzed. Based on the analysis, we focused on the function of ZmMPK4. ZmMPK4 is a two-copy gene and exists as gene pair with ZmMPK3. ZmMPK4 plays a role in ABA signaling. The main results are as follows:
(1) Using database BLAST and Stand-alone BLAST, we identified 19 MAPK genes in the maize genome. The amino acids of 19 MAPK proteins are between 369 and 642. The molecular weight of 19 MAPK proteins are between 42.199 kDa and 72.444 kDa. The pI of 19 MAPK proteins are between 5.26 and 9.82. Four of the 19 MAPK genes exist in chromosome 6 or 8. Three exist in chromosome 5 or 9. Two exist in chromosome 10. One exists in chromosome 1, 3 or 4. The maize MAPKs share more evolutionary relationship with rice MAPKs than Arabidopsis or poplar MAPKs.
(2) ZmMPK1 shares a high sequence similarity with ZmMPK2. There is no EST sequence specifically matches ZmMPK1 sequence. RT-PCR analysis shows that there is not detectable mRNA in roots, stems or leaves of maize seedlings, suggesting ZmMPK1 might be a pseudogene. Other 18 genes can be detected in roots, stems or leaves of maize seedlings. In addition to ZmMPK12, ZmMPK18 and ZmMPK19, other 15 genes expressed in different level.
(3) PCR analysis shows that the band of ZmMPK4 did not match the band of previously reported ZmMPK4 (ZmMPK4-2 in our study). ZmMPK4-2 is a alternative transcript of ZmMPK4 gene that can take alternative splicing. Gene sequence and MAPK gene family analysis revealed that ZmMPK4 is a two-copy gene and exists as gene pair with ZmMPK3. Southern blot showed ZmMPK4 is a two-copy gene. The nucleotide sequences of ZmMPK3 and ZmMPK4 share similarity of 92.1%. The amino acid sequences of ZmMPK3 and ZmMPK4 share similarity of 90.0%. ZmMPK3 and ZmMPK4 are located on the short arm of chromosome 1 and the long arm of chromosome 9, respectively. Both ZmMPK3 and ZmMPK4 could generate mRNA and proteins.
(4) The third intron of ZmMPK4 gene is GC-AG type. ZmMPK4-2 is one alternative transcript result from retention of the third intron of ZmMPK4 gene. The transcript of ZmMPK4-2 is low and mainly found in maize leaves. Another alternative transcript, the main transcript, of ZmMPK4 gene is ZmMPK4-1 without the third intron. The third intron of ZmMPK3 gene is GT-AG type.
(5) Northern blot analysis indicated that ZmMPK3 is mainly expressed in leaves of 5-d-old seedlings and ZmMPK4 in roots. ABA (100 ?M) or NaCl (200 mM) up-regulated the expression of both ZmMPK3 and ZmMPK4 with different patterns. Northern blot analysis did not differentiate the expression of ZmMPK4-1 and ZmMPK4-2. RT-PCR using specific primers revealed that the alternative splicing predominantly occurred in leaves of 5-d-old seedlings. The alternative splicing is regulated by ABA or NaCl.
(6) ZmMPK3 antibody (Anti-ZmMPK3) was generated. Generation of specific antibodies for ZmMPK3 and ZmMPK4 is impossible because of the high similarity of amino acid. In leaves of 5-d-old seedlings, Anti-ZmMPK3 could detect protein band with an approximate molecular mass of 43 kDa. The protein amount could slightly be induced by ABA (100 ?M). Immunoprecipitation assay showed that ABA (100 ?M) stimulates a rapid activation of the 43 kDa protein in 0.5 h or 1 h. Transient expression in Nicotiana benthamiana was performed to specifically examine the kinase activities of ZmMPK3, ZmMPK4-1 or ZmMPK4-2. The results showed that ABA (100 ?M) activated ZmMPK3 or ZmMPK4-1, but not ZmMPK4-1 in 0.5 h, 1 h or 2 h.
(7) Transiently expressing of 35S-GFP-ZmMPK fusion proteins suggest that ZmMPK3 or ZmMPK4-1 fusion protein localized in cell membrane and nucleus, and ZmMPK4-2 fusion protein localized in cell membrane and cytoplasm. These results indicate the insertion of 30 amino acids may disturb the localization of ZmMPK4 protein.
(8) Overexpressing of ZmMPK4-1 in Arabidopsis accelerated stem development. In the adult plants, the rosette leaves arose from the stem and can form stem subsequently. The wild-type and ZmMPK4-1-overexpressing Arabidopsis showed no difference in germination (about 100%) on MS media without ABA treatment. ABA (0.5 ?M) inhibited the germination of both wild-type and ZmMPK4-1-overexpressing seeds. The inhibition effect of ABA on ZmMPK4-1-overexpressing seeds was stronger than that of ABA on wild-type seeds. Immunoprecipitation assay showed anti-p-ERK could detect kinase activity in ZmMPK4-1-overexpressing plants under normal growth conditions. ABA (0.5 ?M) stimulates activation of ZmMPK4-1 in 30 min. AtACT1 is upregulated in ZmMPK4-1-overexpressing plants under light growth conditions. Furthermore, in ZmMPK4-1-overexpressing plants, ABA-inducted AtACT2, ABI3 or ABI5 expression was enhanced.
引文
宋东辉,宋凤鸣,郑重。MAP激酶在植物信号传递网络中的功能。浙江大学学报。2004,(30):119-126
孙大业,郭艳林,马力耕,崔素娟。细胞信号转导。科学出版社。2001 肖文娟,宾金华,武波。植物体中的MAPK。植物学通报。2004,(21):205-215
张腾国,刘玉冰,夏小慧。植物MAP激酶级联途径研究进展。西北植物学报。2008, (28):1704-1714
赵琳琳,徐启江,姜勇,李玉花。生物和非生物胁迫下的植物细胞中丝裂原活化蛋白激酶(MAPK)信号转导。植物生理学通讯。2008,(44):196-174
Abrash E. B. and Bergmann D. C.. Regional specification of stomatal production by the putative ligand CHALLAH. Development. 2010, (137): 447-455
Agrawal G. K., Rakwal R. and Iwahashi H.. Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochem. Biophys. Res. Commun.. 2002, (294): 1009-1016
Ahlfors R., Macioszek V., Rudd J., Brosche M., Schlichting R., Scheel D. and Kangasjarvi J.. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J.. 2004 (40): 512-522
Alexandrov N. N., Brover V. V., Freidin S., Troukhan M. E., Tatarinova T. V., Zhang H., Swaller T. J., Lu Y. P. et al.. Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol. Biol..2009, (69): 179-194
Aloni R., Aloni E., Langhans M. and Ullrich C. I.. Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann. Bot.. 2006, (97): 883-893
Banno H., Hirano K., Nakamura T., Irie K., Nomoto S., Matsumoto K. and Machida Y.. NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases. Mol. Cell. Biol.. 1993, (13): 4745-4752
Banuelos G. S., Fakra S. C., Walse S. S., Marcus M. A., Yang S. I., Pickering I. J., Pilon-Smits E. A. and Freeman J. L.. Selenium accumulation, distribution, and speciation in spineless prickly pear cactus: a drought- and salt-tolerant, selenium-enriched nutraceutical fruit crop for biofortified foods. Plant Physiol.. 2011, (155): 315-327
Bartels S., Gonzalez Besteiro M. A., Lang D. and Ulm R.. Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci.. 2010, (15): 322-329
Beck M., Komis G., Muller J., Menzel D. and Samaj J.. Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell. 2010a, (22): 755-771
Beck M., Komis G., Ziemann A., Menzel D. and Samaj J.. Mitogen-activated protein kinase 4is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol.. 2010b, (189): 1069-1083
Berberich T., Sano H. and Kusano T.. Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol. Gen. Genet.. 1999, (262): 534-542
Bergmann D. C., Lukowitz W. and Somerville C. R.. Stomatal development and pattern controlled by a MAPKK kinase. Science. 2004, (304): 1494-1497
Blanc G., Hokamp K. and Wolfe K. H.. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res.. 2003, (13): 137-144
Blanc G. and Wolfe K. H.. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell. 2004, (16): 1679-1691
Blanco E., Rojas R., Haeger P., Cuevas R., Perez C., Munita R., Quiroz G., Andres M. E. et al.. Intron retention as an alternative splice variant of the rat urocortin 1 gene. Neuroscience. 2006a, (140): 1245-1252
Blanco F. A., Zanetti M. E., Casalongue C. A. and Daleo G. R.. Molecular characterization of a potato MAP kinase transcriptionally regulated by multiple environmental stresses. Plant Physiol. Biochem.. 2006b, (44): 315-322
Bogre L., Ligterink W., Meskiene I., Barker P. J., Heberle-Bors E., Huskisson N. S. and Hirt H.. Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell, 1997, (9): 75-83
Bogre L., Meskiene I., Heberle-Bors E. and Hirt H.. Stressing the role of MAP kinases in mitogenic stimulation. Plant Mol. Biol.. 2000, (43): 705-718
Boonsirichai K., Guan C., Chen R. and Masson P. H.. Root gravitropism: an experimental tool to investigate basic cellular and molecular processes underlying mechanosensing and signal transmission in plants. Annu. Rev. Plant Biol.. 2002, (53): 421-447
Brock A. K., Willmann R., Kolb D., Grefen L., Lajunen H. M., Bethke G., Lee J., Nurnberger T. et al.. The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol.. 2010, (153): 1098-1111
Brosius J.. Retroposons--seeds of evolution. Science. 1991, (251): 753
Cameron S. J., Abe J., Malik S., Che W. and Yang J.. Differential role of MEK5alpha and MEK5beta in BMK1/ERK5 activation. J. Biol. Chem.. 2004, (279): 1506-1512
Carraro N., Forestan C., Canova S., Traas J. and Varotto S.. ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol.. 2006, (142): 254-264
Castells E., Puigdomenech P. and Casacuberta J. M.. Regulation of the kinase activity of the MIK GCK-like MAP4K by alternative splicing. Plant Mol. Biol.. 2006, (61): 747-756
Champion A., Picaud A. and Henry Y.. Reassessing the MAP3K and MAP4K relationships. Trends Plant Sci.. 2004, (9): 123-129
Chang L. and Karin M.. Mammalian MAP kinase signalling cascades. Nature. 2001, (410): 37-40
Chen P. Y., Lee K. T., Chi W. C., Hirt H., Chang C. C. and Huang H. J. Possible involvement of MAP kinase pathways in acquired metal-tolerance induced by heat in plants. Planta. 2008, (228): 499-509
Chinnusamy V., Zhu J. and Zhu J. K.. Cold stress regulation of gene expression in plants. Trends Plant Sci.. 2007, (12): 444-451
Chou W. C., Huang Y. W., Tsay W. S., Chiang T. Y., Huang D. D. and Huang H. J.. Expression of genes encoding the rice translation initiation factor, eIF5A, is involved in developmental and environmental responses. Physiol. Plant.. 2004, (121): 50-57
Colcombet J. and Hirt H.. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem. J.. 2008, (413): 217-226
Cutler S. R., Rodriguez P. L., Finkelstein R. R. and Abrams S. R.. Abscisic acid: emergence of a core signaling network. Annu. Re.v Plant Biol.. 2010, (61): 651-679
De Smet I., Zhang H., Inze D. and Beeckman T.. A novel role for abscisic acid emerges from underground. Trends Plant Sci.. 2006, (11): 434-439
De Vleesschauwer D., Yang Y., Cruz C. V. and Hofte M.. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol.. 2010, (152): 2036-2052 del Pozo O., Pedley K. F. and Martin G. B.. MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO J.. 2004, (23): 3072-3082
Ding H., Tan M., Zhang C., Zhang Z., Zhang A. and Kang Y.. Hexavalent chromium (VI) stress induces mitogen-activated protein kinase activation mediated by distinct signal molecules in roots of Zea mays L. Environ. and Experi. Botany..2009a, (67): 328-334
Ding H., Zhang A., Wang J., Lu R., Zhang H., Zhang J. and Jiang M.. Identity of an ABA-activated 46 kDa mitogen-activated protein kinase from Zea mays leaves: partial purification, identification and characterization. Planta. 2009b, (230): 239-251
Dinga H., Tanb M., Zhangb C., Zhang Z., Zhang A. and Kang Y.. Hexavalent chromium (VI) stress induces mitogen-activated protein kinase activation mediated by distinct signal molecules in roots of Zea mays L. Environ. and Experi. Botany.. 2009, (67): 328-334
Dolgin E.. Maize genome mapped. Nature. 2009, (published online 19 November)
Dombrowski J. E., Hind S. R., Martin R. C. and Stratmann J. W.. Wounding systemically activates a mitogen-activated protein kinase in forage and turf grasses. Plant Sci.. 2011, (180): 686-693
Dong J. and Bergmann D. C.. Stomatal patterning and development. Curr. Top. De.v Biol.. 2010, (91): 267-297
Droillard M., Boudsocq M., Barbier-Brygoo H. and Lauriere C.. Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett.. 2002, (527): 43-50
Droillard MJ., Boudsocq M., Barbier-Brygoo H. and Lauriere C.. Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett.. 2004, (574): 42-48
Emrich S. J., Aluru S., Fu Y., Wen T. J., Narayanan M., Guo L., Ashlock D. A. and Schnable P. S.. A strategy for assembling the maize (Zea mays L.) genome. Bioinformatics. 2004, (20): 140-147
Fiil B. K., Petersen K., Petersen M. and Mundy J.. Gene regulation by MAP kinase cascades. Cur.r Opin. Plant Biol.. 2009 (12): 615-621
Fu S. F., Chou W. C., Huang D. D. and Huang H. J.. Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol.. 2002, (43): 958-963
Fujii H. and Zhu J. K.. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl. Acad Sci. U. S. A.. 2009, (106): 8380-8385
Gao L. and Xiang C. B.. The genetic locus At1g73660 encodes a putative MAPKKK and negatively regulates salt tolerance in Arabidopsis. Plant Mol. Biol.. 2008, (67): 125-134
Ghawana S., Kumar S. and Ahuja P. S.. Early low-temperature responsive mitogen activated protein kinases RaMPK1 and RaMPK2 from Rheum australe D. respond differentially to diverse stresses. Mol. Bio.l Rep.. 2010, (37): 933-938
Gomi K., Ogawa D., Katou S., Kamada H., Nakajima N., Saji H., Soyano T., Sasabe M. et al.. A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol.. 2005, (46): 1902-1914
Gu L., Liu Y., Zong X., Liu L., Li D. P. and Li D. Q.. Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol. Biol. Rep.. 2010, (37): 4067-4073
Gudesblat G. E., Iusem N. D. and Morris P. C.. Guard cell-specific inhibition of Arabidopsis MPK3 expression causes abnormal stomatal responses to abscisic acid and hydrogen peroxide. New Phytol.. 2007, (173): 713-721
Guerra-Peraza O., Nguyen H. T., Stamp P. and Leipner J.. ZmCOI6.1, a novel, alternatively spliced maize gene, whose transcript level changes under abiotic stress. Plant Sci.. 2009, (176): 783-791
Gupta M., Sharma P., Sarin N. B. and Sinha A. K.. Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere. 2009, (74): 1201-1208
Gupta S., Barrett T., Whitmarsh A. J., Cavanagh J., Sluss H. K., Derijard B. and Davis R. J.. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J.. 1996, (15): 2760-2770
Gupta S., Wang B. B., Stryker G. A., Zanetti M. E. and Lal S. K.. Two novel arginine/serine (SR) proteins in maize are differentially spliced and utilize non-canonical splice sites.Biochim. Biophys. Acta.. 2005, (1728): 105-114
Gustin MC., Albertyn J., Alexander M. and Davenport K.. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Bio.l Rev.. 1998, (62): 1264-1300
Guyot R. and Keller B.. Ancestral genome duplication in rice. Genome. 2004, (47): 610-614 Hamel L. P., Nicole M. C., Sritubtim S., Morency M. J., Ellis M., Ehlting J., Beaudoin N., Barbazuk B. et al.. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci..2006, (11): 192-198
Hara K., Kajita R., Torii K. U., Bergmann D. C. and Kakimoto T.. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev.. 2007, (21): 1720-1725
Hashimoto M., Negi J., Young J., Israelsson M., Schroeder J. I. and Iba K.. Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat. Cell Biol.. 2006, (8): 391-397
He C., Fong S. H., Yang D. and Wang G. L.. BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice. Mol. Plant Microbe. Interact.. 1999, (12): 1064-1073
Holding D. R., Meeley R. B., Hazebroek J., Selinger D., Gruis F., Jung R. and Larkins B. A. Identification and characterization of the maize arogenate dehydrogenase gene family. J. Exp. Bot.. 2010, (61): 3663-3673
Hotokezaka H., Sakai E., Kanaoka K., Saito K., Matsuo K., Kitaura H., Yoshida N. and Nakayama K.. U0126 and PD98059, specific inhibitors of MEK, accelerate differentiation of RAW264.7 cells into osteoclast-like cells. J. Biol. Chem.. 2002, (277): 47366-47372
Huang T. L. and Huang H. J.. ROS and CDPK-like kinase-mediated activation of MAP kinase in rice roots exposed to lead. Chemosphere. 2008, (71): 1377-1385
Hubbard K. E., Nishimura N., Hitomi K., Getzoff E. D. and Schroeder J. I.. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev.. 2010, (24): 1695-1708
Hung W. C., Huang D. D., Chien P. S., Yeh C. M., Chen P. Y., Chi W. C. and Huang H. J.. Protein tyrosine dephosphorylation during copper-induced cell death in rice roots. Chemosphere. 2007, (69): 55-62
Hunt L., Bailey K. J. and Gray J. E.. The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol.. 2010a, (186): 609-614
Hunt L. and Gray J. E.. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol.. 2009, (19): 864-869
Hunt L. and Gray J. E.. BASL and EPF2 act independently to regulate asymmetric divisions during stomatal development. Plant Signal. Behav.. 2010b, (5): 278-280
Hurles M.. Gene duplication: the genomic trade in spare parts. PLoS Biol.. 2004, (2): E206 Hwa C. M. and Yang X. C.. The AtMKK3 pathway mediates ABA and salt signaling inArabidopsis. Acta. Physiol. Plant..2008, (30): 277-286
Ichimura K., Mizoguchi T., Irie K., Morris P., Giraudat J., Matsumoto K. and Shinozaki K.. Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem. Biophys. Res. Commun.. 1998, (253): 532-543
Ichimura K., Mizoguchi T., Yoshida R., Yuasa T. and Shinozaki K.. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J.. 2000, (24): 655-665
Ishikawa M., Soyano T., Nishihama R. and Machida Y.. The NPK1 mitogen-activated protein kinase kinase kinase contains a functional nuclear localization signal at the binding site for the NACK1 kinesin-like protein. Plant J.. 2002, (32): 789-798
Jammes F., Song C., Shin D., Munemasa S., Takeda K., Gu D., Cho D., Lee S. et al.. MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc. Natl. Acad. Sci. U. S. A.. 2009, (106): 20520-20525
Jin H., Axtell M. J., Dahlbeck D., Ekwenna O., Zhang S., Staskawicz B. and Baker B.. NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. Dev. Cell. 2002, (3): 291-297
Jonak C., Kiegerl S., Ligterink W., Barker P. J., Huskisson N. S. and Hirt H.. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. U. S. A.. 1996, (93): 11274-11279
Jonak C., Nakagami H. and Hirt H.. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol.. 2004, (136): 3276-3283
Jordan T., Schornack S. and Lahaye T.. Alternative splicing of transcripts encoding Toll-like plant resistance proteins-what's the functional relevance to innate immunity? Trends Plant Sci.. 2002, (7): 392-398
Jouannic S., Champion A., Segui-Simarro J. M., Salimova E., Picaud A., Tregear J., Testillano P., Risueno M. C. et al.. The protein kinases AtMAP3Kepsilon1 and BnMAP3Kepsilon1 are functional homologues of S. pombe cdc7p and may be involved in cell division. Plant J.. 2001, (26): 637-649
Karro J. E., Yan Y., Zheng D., Zhang Z., Carriero N., Cayting P., Harrrison P. and Gerstein M.. Pseudogene.org: a comprehensive database and comparison platform for pseudogene annotation. Nucleic Acids Res.. 2007, (35): 55-60
Kieber J. J., Rothenberg M., Roman G., Feldmann K. A. and Ecker J. R.. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993 (72):427-441
Kiegerl S., Cardinale F., Siligan C., Gross A., Baudouin E., Liwosz A., Eklof S., Till S. et al.. SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell. 2000, (12): 2247-2258
Kim E., Goren A. and Ast G.. Alternative splicing: current perspectives. Bioessays. 2008, (30): 38-47
Kim J. A., Agrawal G. K., Rakwal R., Han K. S., Kim K. N., Yun C. H., Heu S., Park S. Y. et al.. Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signalling pathways and development. Biochem. Biophys. Res. Commun.. 2003, (300): 868-876
Klingler J. P., Batelli G. and Zhu J. K.. ABA receptors: the START of a new paradigm in phytohormone signalling. J. Exp. Bot.. 2010, (61): 3199-3210
Kondo T., Kajita R., Miyazaki A., Hokoyama M., Nakamura-Miura T., Mizuno S., Masuda Y., Irie K. et al.. Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol.. 2010, (51): 1-8
Kong H., Landherr L. L., Frohlich M. W., Leebens-Mack J., Ma H. and dePamphilis C. W.. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J.. 2007, (50): 873-885
Koo S. C., Choi M. S., Chun H. J., Park H. C., Kang C. H., Shim S. I., Chung J. I., Cheong Y. H. et al.. Identification and characterization of alternative promoters of the rice MAP kinase gene OsBWMK1. Mol. Cells. 2009, (27): 467-473
Koo S. C., Yoon H. W., Kim C. Y., Moon B. C., Cheong Y. H., Han H. J., Lee S. M., Kang K. Y. et al.. Alternative splicing of the OsBWMK1 gene generates three transcript variants showing differential subcellular localizations. Biochem. Biophys. Res. Commun.. 2007, (360): 188-193
Koornneef M., Bentsink L. and Hilhorst H.. Seed dormancy and germination. Curr. Opin. Plant Biol.. 2002, (5): 33-36
Kosetsu K., Matsunaga S., Nakagami H., Colcombet J., Sasabe M., Soyano T., Takahashi Y., Hirt H. et al.. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell. 2010, (22): 3778-3790
Kriventseva E. V., Koch I., Apweiler R., Vingron M., Bork P., Gelfand M. S. and Sunyaev S.. Increase of functional diversity alternative splicing. Trends Genet.. 2003, (19): 124-128
Krysan P. J., Jester P. J., Gottwald J. R. and Sussman M. R.. An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis. Plant Cell. 2002, (14): 1109-1120
Lal S., Choi J. H., Shaw J. R. and Hannah L. C.. A splice site mutant of maize activates cryptic splice sites, elicits intron inclusion and exon exclusion, and permits branch point elucidation. Plant Physiol.. 1999, (121): 411-418
Lampard G. R.. The missing link?: Arabidopsis SPCH is a MAPK specificity factor that controls entry into the stomatal lineage. Plant Signal. Behav.. 2009, (4): 425-427
Lampard G. R., Macalister C. A. and Bergmann D. C.. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science. 2008, (322): 1113-1116
Lee J. S. and Ellis B. E.. Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs. J. Biol. Chem.. 2007, (282): 25020-25029
Lee S., Hirt H. and Lee Y.. Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J.. 2001, (26): 479-486
Lin C. W., Chang H. B. and Huang H. J.. Zinc induces mitogen-activated protein kinase activation mediated by reactive oxygen species in rice roots. Plant Physiol. Biochem.. 2005, (43): 963-968
Lin C. W., Lin C. Y., Chang C. C., Lee R. H., Tsai T. M., Chen P. Y., Chi W. C. and Huang H. J.. Early signalling pathways in rice roots under vanadate stress. Plant Physiol. Biochem.. 2009a, (47): 369-376
Lin F., Ding H., Wang J., Zhang H., Zhang A., Zhang Y., Tan M., Dong W. et al.. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot.. 2009b, (60): 3221-3238
Lin W. Y., Matsuoka D., Sasayama D. and Nanmori T.. A splice variant of Arabidopsis mitogen-activated protein kinase and its regulatory function in the MKK6-MPK13 pathway. Plant Sci.. 2010, (178): 245-250
Link V., Sinha A. K., Vashista P., Hofmann M. G., Proels R. K., Ehness R. and Roitsch T.. A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response. FEBS Lett.. 2002, (531): 179-183
Liu P. F., Chang W. C., Wang Y. K., Chang H. Y. and Pan R. L.. Signaling pathways mediating the suppression of Arabidopsis thaliana Ku gene expression by abscisic acid. Biochim. Biophys. Acta.. 2008a, (1779): 164-174
Liu Y. K., Liu Q. Z., Xing X. and Li D. Q.. Effects of MAPKK inhibitor PD98059 on the gravitropism of primary roots of maize. Plant Growth Regul.. 2008b, (59): 191-198
Liu Y. K., Liu Y. B., Zhang M. Y. and Li D. Q.. Stomatal development and movement: The roles of MAPK signaling. Plant Signal. Behav.. 2010, (5): 1176-1180
Lu C., Han M. H., Guevara-Garcia A. and Fedoroff N.V.. Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc. Natl. Acad. Sci. U. S. A.. 2002, (99): 15812-15817
Lukowitz W., Roeder A., Parmenter D. and Somerville C.. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell. 2004, (116): 109-119
Ma Y., Szostkiewicz I., Korte A., Moes D., Yang Y., Christmann A. and Grill E.. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009, (324): 1064-1068
MacAlister C. A., Ohashi-Ito K. and Bergmann D. C.. Transcription factor control asymmetric cell divisions that establish the stomatal lineage. Nature. 2007, (445): 537-540 MacRobbie E. A. and Kurup S.. Signalling mechanisms in the regulation of vacuolar ion release in guard cells. New Phytol.. 2007, (175): 630-640
MAPK Group.. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci.. 2002, (7): 301-308
Mehlmer N., Wurzinger B., Stael S., Hofmann-Rodrigues D., Csaszar E., Pfister B., Bayer R. and Teige M.. The Ca2+-dependent protein kinase CPK3 is required for
MAPK-independent salt-stress acclimation in Arabidopsis. Plant J.. 2010, (63): 484-498
Melcher K., Zhou X. E. and Xu H. E.. Thirsty plants and beyond: structural mechanisms of abscisic acid perception and signaling. Curr. Opin. Struct. Biol.. 2010, (20): 722-729
Melech-Bonfil S. and Sessa G.. Tomato MAPKKKepsilon is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J.. 2010, (64): 379-391
Melikant B., Giuliani C., Halbmayer-Watzina S., Limmongkon A., Heberle-Bors E. and Wilson C.. The Arabidopsis thaliana MEK AtMKK6 activates the MAP kinase AtMPK13. FEBS Lett.. 2004, (576): 5-8
Michael I. P., Kurlender L., Memari N., Yousef G. M., Du D., Grass L., Stephan C., Jung K. et al.. Intron retention: a common splicing event within the human kallikrein gene family. Clin. Chem.. 2005, (51): 506-515
Mikolajczyk M., Awotunde O. S., Muszynska G., Klessig D. F. and Dobrowolska G.. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell. 2000, (12): 165-178
Miles G. P., Samuel M. A., Zhang Y. and Ellis B. E.. RNA interference-based (RNAi) suppression of AtMPK6, an Arabidopsis mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3. Environ. Pollut.. 2005, (138): 230-237
Mizoguchi T., Irie K., Hirayama T., Hayashida N., Yamaguchi-Shinozaki K., Matsumoto K. and Shinozaki K.. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A.. 1996, (93): 765-769
Monroe-Augustus M., Zolman B. K. and Bartel B.. IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell. 2003, (15): 2979-2991
Mousley C. J., Tyeryar K. R., Vincent-Pope P. and Bankaitis V. A.. The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking. Biochim. Biophys. Acta.. 2007, (1771): 727-736
Muller J., Beck M., Mettbach U., Komis G., Hause G., Menzel D. and Samaj J.. Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J.. 2010, (61): 234-248
Munnik T., Ligterink W., Meskiene I. I., Calderini O., Beyerly J., Musgrave A. and Hirt H.. Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. Plant J.. 1999, (20): 381-388
Nakagami H., Kiegerl S. and Hirt H.. OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J. Biol. Chem.. 2004, (279): 26959-26966
Nakamura Y., Tanaka K. J., Miyauchi M., Huang L., Tsujimoto M. and Matsumoto K.. Translational repression by the oocyte-specific protein P100 in Xenopus. Dev. Biol.. 2010, (344): 272-283
Nambara E. and Marion-Poll A.. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol.. 2005, (56): 165-185
Ner-Gaon H., Halachmi R., Savaldi-Goldstein S., Rubin E., Ophir R. and Fluhr R.. Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J.. 2004, (39): 877-885
Nicole M. C., Hamel L. P., Morency M. J., Beaudoin N., Ellis B. E. and Seguin A.. MAP-ping genomic organization and organ-specific expression profiles of poplar MAP kinases and MAP kinase kinases. BMC Genomics. 2006, (7): 223
Nilsen T. W. and Graveley B. R.. Expansion of the eukaryotic proteome by alternative splicing. Nature, 2010, (463): 457-463
Ning J., Li X., Hicks L. M. and Xiong L.. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol.. 2010, (152): 876-890
Nishihama R., Banno H., Kawahara E., Irie K. and Machida Y.. Possible involvement of differential splicing in regulation of the activity of Arabidopsis ANP1 that is related to mitogen-activated protein kinase kinase kinases (MAPKKKs). Plant J.. 1997, (12): 39-48
Nishihama R., Ishikawa M., Araki S., Soyano T., Asada T. and Machida Y.. The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev.. 2001, (15): 352-363
Nishihama R., Soyano T., Ishikawa M., Araki S., Tanaka H., Asada T., Irie K., Ito M. et al.. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell. 2002, (109): 87-99
Oliferenko S., Chew T. G. and Balasubramanian M. K.. Positioning cytokinesis. Genes Dev.. 2009, (23): 660-674
Ortiz-Masia D., Perez-Amador M. A., Carbonell J. and Marcote M. J.. Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. FEBS Lett.. 2007, (581): 1834-1840
Ortiz-Masia D., Perez-Amador M. A., Carbonell P., Aniento F., Carbonell J. and Marcote M. J.. Characterization of PsMPK2, the first C1 subgroup MAP kinase from pea (Pisum sativum L.). Planta. 2008, (227): 1333-1342
Park S. Y., Fung P., Nishimura N., Jensen D. R., Fujii H., Zhao Y., Lumba S., Santiago J. et al.. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science. 2009, (324): 1068-1071
Park YS., Kunze S., Ni X., Feussner I. and Kolomiets M. V.. Comparative molecular andbiochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta. 2010, (231): 1425-1437
Pillitteri L. J., Sloan D. B., Bogenschutz N. L. and Torii K. U.. Termination of asymmetric cell division and differentiation of stomata. Nature, 2007, (445): 501-505
Pitzschke A. and Hirt H.. Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol.. 2006, (141): 351-356
Pitzschke A. and Hirt H.. Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol.. 2009a, (149): 606-615
Pitzschke A., Schikora A. and Hirt H.. MAPK cascade signalling networks in plant defence. Curr. Opin. Plant Biol.. 2009b, (12): 421-426
Pollard T. D.. Mechanics of cytokinesis eukaryotes. Curr. Opin. Cell Bio.. 2010, (22): 50-56
Quettier A. L., Bertrand C., Habricot Y., Miginiac E., Agnes C., Jeannette E. and Maldiney R.. The phs1-3 mutation in a putative dual-specificity protein tyrosine phosphatase gene provokes hypersensitive responses to abscisic acid in Arabidopsis thaliana. Plant J.. 2006, (47): 711-719
Raes J., Vandepoele K., Simillion C., Saeys Y. and Van de Peer Y.. Investigating ancient duplication events in the Arabidopsis genome. J. Struct. Funct. Genomics. 2003, (3): 117-129
Rao K. P., Richa T., Kumar K., Raghuram B. and Sinha A. K.. In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res.. 2010a, (17): 139-153
Rao K. P., Vani G., Kumar K., Wankhede D. P., Misra M., Gupta M. and Sinha A. K.. Arsenic stress activates MAP kinase in rice roots and leaves. Arch. Biochem. Biophys.. 2010b, (506): 73-82 Rodriguez M. C., Petersen M. and Mundy J.. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol.. 2010, (61): 621-649
Rowe M. H. and Bergmann D. C.. Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development. Curr. Opin. Plant Biol.. 2010, (13): 548-555
Samuel M. A. and Ellis B. E.. Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell. 2002, (14): 2059-2069
Samuel M. A., Miles G. P. and Ellis B. E.. Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J.. 2000, (22): 367-376
Sangwan V., Orvar BL., Beyerly J., Hirt H. and Dhindsa R. S.. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J.. 2002, (31): 629-638
Sankoff D.. Gene and genome duplication. Curr. Opin. Genet. Dev.. 2001, (11): 681-684
Sasabe M., Soyano T., Takahashi Y., Sonobe S., Igarashi H., Itoh TJ., Hidaka M. and Machida Y.. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev.. 2006, (20): 1004-1014
Schnable P. S., Ware D., Fulton R. S., Stein J. C., Wei F., Pasternak S., Liang C., Zhang J. et al.. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009, (326): 1112-1115
Schweighofer A., Kazanaviciute V., Scheikl E., Teige M., Doczi R., Hirt H., Schwanninger M., Kant M. et al.. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell. 2007, (19): 2213-2224
Seo S., Sano H. and Ohashi Y.. Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell. 1999, (11): 289-298
Serna L.. Stomatal development in Arabidopsis and grasses: differences and commonalities. Int. J. Dev. Biol.. 2011, (55): 5-10
Seyfried J., Wang X., Kharebava G. and Tournier C.. A novel mitogen-activated protein kinase docking site in the N terminus of MEK5alpha organizes the components of the extracellular signal-regulated kinase 5 signaling pathway. Mol. Cell. Biol.. 2005, (25): 9820-9828
Sheth N., Roca X., Hastings M. L., Roeder T., Krainer A. R. and Sachidanandam R.. Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res.. 2006, (34): 3955-3967
Shi J., An H. L., Zhang L., Gao Z. and Guo X. Q.. GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol. Biol.. 2011, (74): 1-17
Soyano T., Ishikawa M., Nishihama R., Araki S., Ito M., Ito M. and Machida Y.. Control of plant cytokinesis by an NPK1-mediated mitogen-activated protein kinase cascade. Philos. Trans R. Soc. Lond. B Biol. Sci.. 2002, (357): 767-775
Soyano T., Nishihama R., Morikiyo K., Ishikawa M. and Machida Y.. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev.. 2003, (17): 1055-1067
Stamm S., Ben-Ari S., Rafalska I., Tang Y., Zhang Z., Toiber D., Thanaraj T. A. and Soreq H.. Function of alternative splicing. Gene, 2005, (344): 1-20
Sudo T., Yagasaki Y., Hama H., Watanabe N. and Osada H.. Exip, a new alternative splicing variant of p38 alpha, can induce an earlier onset of apoptosis in HeLa cells. Biochem. Biophys. Res. Commun.. 2002, (291): 838-843
Sugano S. S., Shimada T., Imai Y., Okawa K., Tamai A., Mori M. and Hara-Nishimura I.. Stomagen positively regulates stomatal density in Arabidopsis. Nature, 2010, (463): 241-244
Suri S. S. and Dhindsa R. S.. A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant Cell Environ.. 2008, (31): 218-226
Swarup R., Kramer E. M., Perry P., Knox K., Leyser H. M., Haseloff J., Beemster G. T., Bhalerao R. et al.. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol.. 2005, (7): 1057-1065
Takahashi F., Mizoguchi T., Yoshida R., Ichimura K. and Shinozaki K.. Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol. Cell. 2011a, (41): 649-660
Takahashi Y., Soyano T., Kosetsu K., Sasabe M. and Machida Y.. HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol.. 2010, (51): 1766-1776
Takahashi Y., Soyano T., Kosetsu K., Sasabe M. and Machida Y.. HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol.. 2011b, (51): 1766-1776
Takahashi Y., Soyano T., Sasabe M. and Machida Y.. A MAP kinase cascade that controls plant cytokinesis. J. Biochem.. 2004, (136): 127-132
Tanaka H., Ishikawa M., Kitamura S., Takahashi Y., Soyano T., Machida C. and Machida Y..
The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells. 2004, (9): 1199-1211
Teige M., Scheikl E., Eulgem T., Doczi R., Ichimura K., Shinozaki K., Dangl J. L. and Hirt H..
The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell. 2004, (15): 141-152
Ulm R., Ichimura K., Mizoguchi T., Peck S. C., Zhu T., Wang X., Shinozaki K. and Paszkowski J.. Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J.. 2002, (21): 6483-6493
Umezawa T., Nakashima K., Miyakawa T., Kuromori T., Tanokura M., Shinozaki K. and Yamaguchi-Shinozaki K.. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol.. 2010, (51): 1821-1839
Umezawa T., Sugiyama N., Mizoguchi M., Hayashi S., Myouga F., Yamaguchi-Shinozaki K., Ishihama Y., Hirayama T. et al.. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A.. 2009, (106): 17588-17593
Wang H., Ngwenyama N., Liu Y., Walker J. C. and Zhang S.. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 2007a, (19): 63-73
Wang J., Ding H., Zhang A., Ma F., Cao J. and Jiang M.. A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverseenvironmental cues. J. Integr. Plant Biol.. 2010a, (52): 442-452
Wang M., Zhang Y., Wang J., Wu X. and Guo X.. A novel MAP kinase gene in cotton (Gossypium hirsutum L.), GhMAPK, is involved in response to diverse environmental stresses. J. Biochem. Mol. Biol.. 2007b, (40): 325-332
Wang W., Zheng H., Fan C., Li J., Shi J., Cai Z., Zhang G., Liu D. et al.. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell. 2006, (18): 1791-1802
Wang X. J., Zhu S. Y., Lu Y. F., Zhao R., Xin Q., Wang X. F. and Zhang D. P.. Two coupled components of the MAP kinase cascade MdMPK1 and MdMKK1 from apple function in ABA signal transduction. Plant Cell Physiol.. 2010b, (51): 754-766
Werneke J. M., Chatfield J. M. and Ogren W. L.. Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell. 1989, (1): 815-825
Xing Y., Jia W. and Zhang J.. AtMEK1 mediates stress gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J. Exp. Bot.. 2007, (58): 2969-2981
Xing Y., Jia W. and Zhang J.. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J.. 2008, (54): 440-451
Xing Y., Jia W. and Zhang J.. AtMKK1 and AtMPK6 are involved in abscisic acid and sugar signaling in Arabidopsis seed germination. Plant Mol. Biol.. 2009, (70): 725-736
Xiong L., Schumaker K. S. and Zhu J. K.. Cell signaling during cold, drought, and salt stress. Plant Cell. 2002, (14 Suppl.): S165-183
Xiong L. and Yang Y.. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell. 2003, (15): 745-759
Xu H., Wang X., Sun X., Shi Q., Yang F. and Du D.. Molecular cloning and characterization of a cucumber MAP kinase gene in response to excess NO3- and other abiotic stresses. Scientia Horticulturae. 2008, (117): 1-8
Yang J. Y., Moulin N., van Bemmelen M. X., Dubuis G., Tawadros T., Haefliger J. A., Waeber G. and Widmann C.. Splice variant-specific stabilization of JNKs by IB1/JIP1. Cell Signal.. 2007, (19): 2201-2207
Yang T., Chaudhuri S., Yang L., Du L. and Poovaiah B. W.. A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J. Biol. Chem.. 2010a, (285): 7119-7126
Yang T., Shad Ali G., Yang L., Du L., Reddy A. S. and Poovaiah B. W.. Calcium/calmodulin -regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal. Behav.. 2010b, (5): 991-994
Yeh C. M., Chien P. S. and Huang H. J.. Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J. Exp. Bot.. 2007, (58): 659-671
Yeh C. M., Hsiao L. J. and Huang H. J.. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol.. 2004, (45): 1306-1312
Yu L., Nie J., Cao C., Jin Y., Yan M., Wang F., Liu J., Xiao Y. et al.. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol.. 2010, (188): 762-773
Yuan S., Wang Y. and Dean J. F.. ACC oxidase genes expressed in the wood-forming tissues of loblolly pine (Pinus taeda L.) include a pair of nearly identical paralogs (NIPs). Gene. 2010, (453): 24-36
Zhang A., Jiang M., Zhang J., Tan M. and Hu X.. Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol.. 2006a, (141): 475-487
Zhang J., Jia W., Yang J. and Ismail A. M.. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research. 2006b, (97): 111–119
Zhang J. Z., Li Z. M., Mei L., Yao J. L. and Hu C. G.. PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuation in expression level. Planta. 2009, (229): 847-859
Zhang S., Liu Y. and Klessig D. F.. Multiple levels of tobacco WIPK activation during the induction of cell death by fungal elicitins. Plant J.. 2000, (23): 339-347
Zhang X., Garreton V. and Chua N. H.. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev.. 2005, (19): 1532-1543
Zhao Z., Zhang W., Stanley B. A. and Assmann S. M.. Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell. 2008, (20): 3210-3226
Zhong S., Lin Z. and Grierson D.. Tomato ethylene receptor-CTR interactions: visualization of NEVER-RIPE interactions with multiple CTRs at the endoplasmic reticulum. J. Exp. Bot.. 2008, (59): 965-972