Overexpressing OsMAPK12-1 inhibits plant growth and enhances resistance to bacterial disease in rice
Xiaorong Xiao A B * , Zhijuan Tang A B * , Xiuqiong Li A B * , Yuhui Hong A B , Boling Li A B , Wenfang Xiao A B , Zhiliang Gao A B , Daozhe Lin A B , Chunxia Li A B , Lijuan Luo A B , Xiaolei Niu A B , Chaozu He A B C and Yinhua Chen A B C
+ Author Affiliations
- Author Affiliations
A Hainan Key Laboratory for Sustainable Utilisation of Tropical Bioresource, Hainan University, Haikou 570228, PR China.
B College of Agriculture, Hainan University, Haikou 570228, PR China.
C Corresponding authors. Emails: yhchen@hainu.edu.cn; czhe@hainu.edu.cn
Functional Plant Biology 44(7) 694-704 https://doi.org/10.1071/FP16397
Submitted: 21 November 2016 Accepted: 29 March 2017 Published: 1 May 2017
Abstract
Mitogen-activated protein kinases (MAPKs) play important roles in plant growth and development, plant abiotic stresses signalling pathway and plant–pathogen interactions. However, little is known about the roles of MAPKs in modulating plant growth and pathogen resistance. In this study, we found that OsMAPK12–1, an alternatively spliced form of BWMK1 in rice (Oryza sativa L.), was induced by various elicitors, such as jasmonic acid, salicylic acid, melatonin and bacterial pathogens. To further investigate the involvement of OsMAPK12–1 in plant growth and stress responses to bacterial pathogens, we constructed OsMAPK12–1 overexpression and knockdown (RNAi) transgenic rice lines. Interestingly, overexpressing OsMAP12–1 inhibited seed germination and seedling growth. Additionally, the OsMAP12-1-overexpression lines displayed enhanced disease resistance against Xanthomonas oryzae pv. oryzae PXO99 and Xanthomonas oryzae pv. oryzicola RS105, whereas the OsMAPK12-1-RNAi lines were more susceptible to these pathogens than wild type. These results suggest that OsMAPK12-1 plays a negative role in plant growth and positively modulates disease resistance against bacterial blight and streak in rice.
Additional keywords: disease resistance, growth inhibition, innate immunity, mitogen-activated protein kinase, rice.
References
Agrawal GK, Rakwal R, Iwahashi H (2002) Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochemical and Biophysical Research Communications 294, 1009–1016.| Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xks1Gnt78%3D&md5=88340e93d57d8ef20b44d04894538cfdCAS |
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983.
| MAP kinase signalling cascade in Arabidopsis innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhsl2lu7c%3D&md5=ff3fb62489ff984cdb85cd13d4298d8fCAS |
Berberich T, Sano H, Kusano T (1999) Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Molecular and General Genetics MGG 262, 534–542.
| Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnvFKrtrg%3D&md5=41c3e1d96c6000b1c69f8e2b4f0f309cCAS |
Berriri S, Garcia AV, Frei dit Frey N, Rozhon W, Pateyron S, Leonhardt N, Montillet JL, Leung J, Hirt H, Colcombet J (2012) Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. The Plant Cell 24, 4281–4293.
| Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKls7vJ&md5=b85e8ed174d055892926d5ed0bc335c9CAS |
Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proceedings of the National Academy of Sciences of the United States of America 106, 8067–8072.
| Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1Whsrk%3D&md5=b6333bb5920e27936d1e19dd65d9eebdCAS |
Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiology 132, 1961–1972.
| BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVantL4%3D&md5=72c0a5b476c61b05c408dda12bdcbf87CAS |
Des Marais DL, Auchincloss LC, Sukamtoh E, McKay JK, Logan T, Richards JH, Juenger TE (2014) Variation in MPK12 affects water use efficiency in Arabidopsis and reveals a pleiotropic link between guard cell size and ABA response. Proceedings of the National Academy of Sciences of the United States of America 111, 2836–2841.
| Variation in MPK12 affects water use efficiency in Arabidopsis and reveals a pleiotropic link between guard cell size and ABA response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFamsrY%3D&md5=5f41319bd4a97593605ca458c5a0ab14CAS |
Fu L, Chen S, Yi J, Hou Z (2014) Effects of different fermentation methods on bacterial cellulose and acid production by Gluconacetobacter xylinus in Cantonese-style rice vinegar. Food Science and Technology International - Cienciay tecnologia de los alimentos internacional 20, 321–331.
He C, Fong SH, Yang D, Wang GL (1999) BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice, molecular plant–microbe interactions. Molecular Plant-Microbe Interactions 12, 1064–1073.
| BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice, molecular plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsFSisrY%3D&md5=3d0212ede7547f4f5e87e70cef9e5eb1CAS |
Hirt H (1997) Multiple roles of MAP kinases in plant signal transduction. Trends in Plant Science 2, 11–15.
| Multiple roles of MAP kinases in plant signal transduction.Crossref | GoogleScholarGoogle Scholar |
Hõrak H, Sierla M, Tõldsepp K, Wang C, Wang YS, Nuhkat M, Valk E, Pechter P, Merilo E, Salojärvi J, Overmyer K, Loog M, Brosché M, Schroeder JI, Kangasjärvi J, Kollist H (2016) A dominant mutation in the HT1 kinase uncovers roles of MAP kinases and GHR1 in CO2-induced stomatal closure. The Plant Cell 28, 2493–2509.
| A dominant mutation in the HT1 kinase uncovers roles of MAP kinases and GHR1 in CO2-induced stomatal closure.Crossref | GoogleScholarGoogle Scholar |
Huang HJ, Fu SF, Tai YH, Chou WC, Huang DD (2002) Expression of Oryza sativa MAP kinase gene is developmentally regulated and stress-responsive. Physiologia Plantarum 114, 572–580.
| Expression of Oryza sativa MAP kinase gene is developmentally regulated and stress-responsive.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFCnt7o%3D&md5=eb5e3821292696bb389fbcefb39e4938CAS |
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases AtMPK4 and AtMPK6. The Plant Journal: for Cell and Molecular Biology 24, 655–665.
Innes RW (2001) Mapping out the roles of MAP kinases in plant defense. Trends in Plant Science 6, 392–394.
| Mapping out the roles of MAP kinases in plant defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvF2htb0%3D&md5=3f54b001d74f7c50ed747f6d74785196CAS |
Jakobson L, Vaahtera L, Tõldsepp K, Nuhkat M, Wang C, Wang YS, Hõrak H, Valk E, Pechter P, Sindarovska Y, et al (2016) Natural variation in Arabidopsis Cvi-0 accession reveals an important role of MPK12 in guard cell CO2 signaling. PLoS Biology 14, e2000322
| Natural variation in Arabidopsis Cvi-0 accession reveals an important role of MPK12 in guard cell CO2 signaling.Crossref | GoogleScholarGoogle Scholar |
Jalmi SK, Sinha AK (2016) Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in rice. Scientific Reports 6, 37974
| Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitFWgtbfN&md5=16049ca43c78300901975ba10df05dbdCAS |
Kauffman HE, Reddy APK, Hsieh SPY, Merca SD (1973) An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Disease Research 57, 537–541.
Khokon MA, Salam MA, Jammes F, Ye W, Hossain MA, Uraji M, Nakamura Y, Mori IC, Kwak JM, Murata Y (2015) Two guard cell mitogen-activated protein kinases, MPK9 and MPK12, function in methyl jasmonate-induced stomatal closure in Arabidopsis thaliana. Plant Biology 17, 946–952.
| Two guard cell mitogen-activated protein kinases, MPK9 and MPK12, function in methyl jasmonate-induced stomatal closure in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlWiu7bM&md5=774b6292b6ff0fbea8fb38bd643b21f4CAS |
Kong Q, Qu N, Gao M, Zhang Z, Ding X, Yang F, Li Y, Dong OX, Chen S, Li X, Zhang Y (2012) The MEKK1–MKK1/MKK2–MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. The Plant Cell 24, 2225–2236.
| The MEKK1–MKK1/MKK2–MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOktb3P&md5=7ca34d027058fbb81dd62d9d628235efCAS |
Koo SC, Yoon HW, Kim CY, Moon BC, Cheong YH, Han HJ, Lee SM, Kang KY, Kim MC, Lee SY, Chung WS, Cho MJ (2007) Alternative splicing of the OsBWMK1 gene generates three transcript variants showing differential subcellular localizations. Biochemical and Biophysical Research Communications 360, 188–193.
| Alternative splicing of the OsBWMK1 gene generates three transcript variants showing differential subcellular localizations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntFamtrs%3D&md5=35b6ae4f13b7e318eb70679ffc1103a8CAS |
Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid, molecular plant–microbe interactions. Molecular Plant-Microbe Interactions 13, 347–351.
| Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid, molecular plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXht1ymurg%3D&md5=3f0c9fd26f7f6d7ff017bfd639fd7a54CAS |
Kyriakis JM, Avruch J (1996) Protein kinase cascades activated by stress and inflammatory cytokines. BioEssays 18, 567–577.
| Protein kinase cascades activated by stress and inflammatory cytokines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvVWktb4%3D&md5=77fb59c7974fca05d1322560b3aa7b3eCAS |
Lee HY, Back K (2016) Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants. Journal of Pineal Research 60, 327–335.
| Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xjs1Gnu74%3D&md5=9f8338a6ee8b75e4f643a96ea769f9b3CAS |
Lee JS, Wang S, Sritubtim S, Chen JG, Ellis BE (2009) Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. The Plant Journal 57, 975–985.
| Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqur4%3D&md5=2ae1d75773255abbba500d266f5a8307CAS |
Lee HY, Byeon Y, Back K (2014) Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. Journal of Pineal Research 57, 262–268.
| Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsF2ntbjP&md5=c341b9856c742b089d636c62a4c42a85CAS |
Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012a) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLOS Genetics 8, e1002767
| Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVWrurY%3D&md5=3077b346383b964c1c09bad15fbcf2ccCAS |
Li Z, Yue H, Xing D (2012b) MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytologist 195, 85–96.
| MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSgsbfK&md5=f511b70714c5864a5ff855584ec03c10CAS |
Liu D, Zhang HT, Xiong W, Hu J, Xu B, Lin CC, Xu L, Jiang L (2014) Effect of temperature on Chinese rice wine brewing with high concentration presteamed whole sticky rice. BioMed Research International 2014, 426929
Lo SF, Fan MJ, Hsing YI, Chen LJ, Chen S, Wen IC, Liu YL, Chen KT, Jiang MJ, Lin MK, Rao MY, Yu LC, Ho TH, Yu SM (2016) Genetic resources offer efficient tools for rice functional genomics research. Plant, Cell & Environment 39, 998–1013.
| Genetic resources offer efficient tools for rice functional genomics research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlvVaitbc%3D&md5=7ae92792340ce9b417e5d38c405819f6CAS |
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annual Review of Phytopathology 51, 245–266.
| MAPK cascades in plant disease resistance signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOhtrvF&md5=42692cbccd8341df15bd84c090520961CAS |
Moustafa K, Lefebvre-De Vos D, Leprince A-S, Savourée A, Laurière C (2008) Analysis of the Arabidopsis mitogen-activated protein kinase families: organ specificity and transcriptional regulation upon water stresses. Scholarly Research Exchange 2008, 143656
| Analysis of the Arabidopsis mitogen-activated protein kinase families: organ specificity and transcriptional regulation upon water stresses.Crossref | GoogleScholarGoogle Scholar |
Ookawa T, Inoue K, Matsuoka M, Ebitani T, Takarada T, Yamamoto T, Ueda T, Yokoyama T, Sugiyama C, Nakaba S, Funada R, Kato H, Kanekatsu M, Toyota K, Motobayashi T, Vazirzanjani M, Tojo S, Hirasawa T (2014) Increased lodging resistance in long-culm, low-lignin gh2 rice for improved feed and bioenergy production. Scientific Reports 4, 6567
| Increased lodging resistance in long-culm, low-lignin gh2 rice for improved feed and bioenergy production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXktlOhtrw%3D&md5=d73fe6a628398f56989e0b39b42dd52cCAS |
Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G, Uhrig J, Weyhe M, Scheel D, Lee J (2014) The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of ‘VQ-motif’-containing proteins to regulate immune responses. New Phytologist 203, 592–606.
| The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of ‘VQ-motif’-containing proteins to regulate immune responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVahtLrJ&md5=5164aea7b405739a2027ebc9ec05ee7dCAS |
Persak H, Pitzschke A (2013) Tight interconnection and multi-level control of Arabidopsis MYB44 in MAPK cascade signaling. PLoS One 8, e57547
| Tight interconnection and multi-level control of Arabidopsis MYB44 in MAPK cascade signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjs12nt7k%3D&md5=e16982b52d2bafd37ca29a952407d9b2CAS |
Pitzschke A, Datta S, Persak H (2014) Salt stress in Arabidopsis: lipid transfer protein AZI1 and its control by mitogen-activated protein kinase MPK3. Molecular Plant 7, 722–738.
| Salt stress in Arabidopsis: lipid transfer protein AZI1 and its control by mitogen-activated protein kinase MPK3.Crossref | GoogleScholarGoogle Scholar |
Reyna NS, Yang Y (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection, molecular plant–microbe interactions. Molecular Plant-Microbe Interactions 19, 530–540.
| Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection, molecular plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVClsLg%3D&md5=ccd35bc12ac3fd12cb72108ee13b347cCAS |
Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annual Review of Plant Biology 61, 621–649.
| Mitogen-activated protein kinase signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslSjsbg%3D&md5=b667095ff6e8b581065b708ea72d90e8CAS |
Sahoo KK, Tripathi AK, Pareek A, Sopory SK, Singla-Pareek SL (2011) An improved protocol for efficient transformation and regeneration of diverse indica rice cultivars. Plant Methods 7, 49
| An improved protocol for efficient transformation and regeneration of diverse indica rice cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVyitLg%3D&md5=cb35cc113d7f3d7e56cc9e72aa004722CAS |
Seo S, Sano H, Ohashi Y (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. The Plant Cell 11, 289–298.
| Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsVyntbg%3D&md5=ba53be0bc2d10cbb0299d5f218c7ea8aCAS |
Seo YS, Chern M, Bartley LE, Han M, Jung KH, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park CJ, Chen X, Hwang S, Jeon JS, Ronald PC (2011) Towards establishment of a rice stress response interactome. PLOS Genetics 7, e1002020
| Towards establishment of a rice stress response interactome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltV2ks7w%3D&md5=b2ef4c862f31cc88ad23645f0b6f876aCAS |
Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC (2013) Recent advances in dissecting stress-regulatory crosstalk in rice. Molecular Plant 6, 250–260.
| Recent advances in dissecting stress-regulatory crosstalk in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWjtbg%3D&md5=87bdd6e5fdf10077812ae76b97c57824CAS |
Shi H, Chen Y, Tan DX, Reiter RJ, Chan Z, He C (2015) Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. Journal of Pineal Research 59, 102–108.
| Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXovVCrsbw%3D&md5=0a94bf950a29ec8bc7c40ebcee84f503CAS |
Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signaling & Behavior 6, 196–203.
| Mitogen-activated protein kinase signaling in plants under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yjsr4%3D&md5=d2ee023fec54e7831809ed1848c2a876CAS |
Song F, Goodman RM (2002) OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta 215, 997–1005.
| OsBIMK1, a rice MAP kinase gene involved in disease resistance responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovValurk%3D&md5=730428b0f6b50a8f739b3c30de720cc5CAS |
Song D, Chen J, Song F, Zheng Z (2006) A novel rice MAPK gene, OsBIMK2, is involved in disease-resistance responses. Plant Biology 8, 587–596.
| A novel rice MAPK gene, OsBIMK2, is involved in disease-resistance responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSktbnN&md5=6a3b22b65818db7579d53259f8fb4288CAS |
Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Molecular Cell 15, 141–152.
| The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeju7g%3D&md5=1de769b5baa12824741e001edcc4aceaCAS |
Tena G, Asai T, Chiu WL, Sheen J (2001) Plant mitogen-activated protein kinase signaling cascades. Current Opinion in Plant Biology 4, 392–400.
| Plant mitogen-activated protein kinase signaling cascades.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFKgtrw%3D&md5=6ca672c90bac520164bba9d82e31e0d7CAS |
Tsuda K, Mine A, Bethke G, Igarashi D, Botanga CJ, Tsuda Y, Glazebrook J, Sato M, Katagiri F (2013) Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLOS Genetics 9, e1004015
| Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. The Plant Cell 19, 63–73.
| Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Wang P, Du Y, Li Y, Ren D, Song CP (2010) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. The Plant Cell 22, 2981–2998.
| Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKjs7rL&md5=df0a21eb332dd4b2a709661f85fef670CAS |
Wei Y, Zeng H, Hu W, Chen L, He C, Shi H (2016) Comparative transcriptional profiling of melatonin synthesis and catabolic genes indicates the possible role of melatonin in developmental and stress responses in rice. Frontiers in Plant Science 7, 676
| Comparative transcriptional profiling of melatonin synthesis and catabolic genes indicates the possible role of melatonin in developmental and stress responses in rice.Crossref | GoogleScholarGoogle Scholar |
Wen JQ, Oono K, Imai R (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiology 129, 1880–1891.
| Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmtl2gtb4%3D&md5=a21a0b7e23afd105a86eedfd9c55eb08CAS |
Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. The Plant Journal 54, 440–451.
| AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Wmsbs%3D&md5=848ccf3470c3634b93e095a1be411e53CAS |
Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. The Plant Cell 15, 745–759.
| Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVektbw%3D&md5=06b5c44ab9c56fd7776e61e7801c5c35CAS |
Xiong L, Lee MW, Qi M, Yang Y (2001) Identification of defense-related rice genes by suppression subtractive hybridization and differential screening, molecular plant–microbe interactions. Molecular Plant-Microbe Interactions 14, 685–692.
| Identification of defense-related rice genes by suppression subtractive hybridization and differential screening, molecular plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivFOrs7s%3D&md5=2d1631b381fe579e44f1bed8c5b286e6CAS |
Xu J, Chua NH (2012) Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation. EMBO Journal 31, 1975–1984.
| Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1eksLk%3D&md5=99e80188eb1e2a3144f278d7eef4c7fbCAS |
Xu J, Zhang S (2015) Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends in Plant Science 20, 56–64.
| Mitogen-activated protein kinase cascades in signaling plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslGnsbjP&md5=212949a3555445ee38a5d2ae5ac64517CAS |
Yin L, Wang P, Li M, Ke X, Li C, Liang D, Wu S, Ma X, Li C, Zou Y, Ma F (2013) Exogenous melatonin improves Malus resistance to Marssonina apple blotch. Journal of Pineal Research 54, 426–434.
| Exogenous melatonin improves Malus resistance to Marssonina apple blotch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtFaksbk%3D&md5=a05ffc534231aa1b62125764f5a1a22aCAS |
Yuan B, Shen X, Li X, Xu C, Wang S (2007) Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta 226, 953–960.
| Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1CntLs%3D&md5=a75765ff15c066c6235ca3d8122e0ae6CAS |
Yuasa T, Ichimura K, Mizoguchi T, Shinozaki K (2001) Oxidative stress activates AtMPK6, an Arabidopsis homologue of MAP kinase. Plant & Cell Physiology 42, 1012–1016.
| Oxidative stress activates AtMPK6, an Arabidopsis homologue of MAP kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntFWksbw%3D&md5=44e81284688d45611815486f14baa149CAS |
Zeng Q, Chen JG, Ellis BE (2011) AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. The Plant Journal 67, 895–906.
| AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFOhsbvE&md5=ad629861260ab2195cae01bf78288dcfCAS |
Zhang S, Klessig DF (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. The Plant Cell 9, 809–824.
| Salicylic acid activates a 48-kD MAP kinase in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtleisrY%3D&md5=2dc2f3a9c43001c1c517ec23cef4b66aCAS |
Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends in Plant Science 6, 520–527.
| MAPK cascades in plant defense signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFGksLk%3D&md5=fa334c5e2252a7ceab10ab3e593300e7CAS |
Zhang C, Zhou L, Zhu Z, Lu H, Zhou X, Qian Y, Li Q, Lu Y, Gu M, Liu Q (2016) Characterization of grain quality and starch fine structure of two Japonica rice (Oryza sativa) cultivars with good sensory properties at different temperatures during the filling stage. Journal of Agricultural and Food Chemistry 64, 48–57.
Zhou J, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2014) RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. Journal of Experimental Botany 65, 595–607.
| RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1ChsLo%3D&md5=3e24fc20d4d6d72a0a1ff7779509e478CAS |
