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Expression pattern and function of wheat mitogen-activated protein kinase (MPK) cascade genes under micronutrient-deprived conditions

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Abstract

Mitogen-activated protein kinase (MAPK) cascades function as conserved signaling modules and play critical roles in mediating plant growth and responses to abiotic stresses. In this study, expression patterns of the genes encoding wheat (Triticum aestivum) MPKKK, MPKK, and MPK proteins and the function of TaMPK4 in mediating plant response to deprived micronutrients were investigated. The wheat MPK cascade proteins harbor conserved motifs shared by their plant counterparts. Expression analysis indicated that TaMPKKK;A, TaMPKKK;3, TaMPKK6, TaMPK3, TaMPK4, TaMPK9, and TaMPK17 exhibited altered transcripts upon distinct micronutrient deprivations, indicating their potential roles in transducing signaling elicited by deprived micronutrients via transcriptional response. Functional analysis on TaMPK4, a MPK gene mediating response to deprived Zn, Mo, and B stresses, indicated its role in mediating plant tolerance to deprived micronutrients. Under Zn, Mo, and B stress treatments, tobacco seedlings overexpressing TaMPK4 exhibited improved phenotype, increased biomass, enhanced activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), and lowered contents of malondialdehyde (MDA) relative to WT, while the TaMPK4 knockdown lines showed deteriorated seedling phenotype, decreased biomass, lowered activities of SOD, CAT, and POD, and increased MDA amount compared with WT. NtSOD2, NtCAT, and NtPOD9, the genes encoding SOD, CAT, and POD, respectively, exhibited modified transcripts in transgenic lines deprived by Zn, Mo, and B, with a pattern to be consistent with the antioxidant enzyme activities. These results indicate that the TaMPK4-mediated plant tolerance to Zn, Mo, and B stresses is associated with this gene function in improving reactive oxygen species (ROS) homeostasis through transcriptionally regulating AE genes. Our results provide insights into expression patterns of the wheat MPK cascade genes under deprived micronutrient conditions and reveal the function of TaMPK4 in modulating plant responses to deprived Zn, Mo, and B stresses which are associated with cellular ROS homeostasis improvement.

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References

  • Agarwal PK, Gupta K, Jha B (2010) Molecular characterization of the Salicornia brachiata SbMAPKK gene and its expression by abiotic stress. Mol Biol Rep 37:981–986

    Article  CAS  PubMed  Google Scholar 

  • Asai S, Yoshioka H (2008) The role of radical burst via MAPK signaling in plant immunity. Plant Signal Behav 3:920–922

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardinale F, Meskiene I, Ouaked F, Hirt H (2002) Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell 14:703–711

    CAS  PubMed  PubMed Central  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226

    Article  CAS  PubMed  Google Scholar 

  • Dai H, Jia G, Shan C (2015) Jasmonic acid-induced hydrogen peroxide activates MEK1/2 in upregulating the redox states of ascorbate and glutathione in wheat leaves. Acta Physiol Plant 37:200

    Article  Google Scholar 

  • Ding HD, Zhang XH, Xu SC, Sun LL, Jiang MY, Zhang AY, Jin YG (2009a) Induction of protection against paraquat-induced oxidative damage by abscisic acid in maize leaves is mediated through mitogen-activated protein kinase. J Integr Plant Biol 51:961–972

    Article  CAS  PubMed  Google Scholar 

  • Ding HD, Tan MP, Zhang C, Zhang ZW, Zhang AY, Kang YJ (2009b) Hexavalent chromium (VI) stress induces mitogen-activated protein kinase activation mediated by distinct signal molecules in roots of Zea mays L. Environ Exp Bot 67:328–334

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gomi K, Ogawa D, Katou S, Kamada H, Nakajima N, Saji H (2005) 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 46:1902–1914

    Article  CAS  PubMed  Google Scholar 

  • Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K (2013) Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237:1163–1178

    Article  CAS  PubMed  Google Scholar 

  • Hao L, Wen Y, Zhao Y, Lu W, Xiao K (2015) Wheat mitogen-activated protein kinase gene TaMPK4 improves plant tolerance to multiple stresses through modifying root growth, ROS metabolism, and nutrient acquisitions. Plant Cell Rep 34:2081–2097

    Article  CAS  PubMed  Google Scholar 

  • Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang XS, Luo T, Fu XZ, Fan QJ, Liu JH (2011) Cloning and molecular characterization of a mitogen-activated protein kinase gene from Poncirus trifoliata whose ectopic expression confers dehydration/drought tolerance in transgenic tobacco. J Exp Bot 62:5191–5206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Wang W, Zhang Q, Liu J (2013) A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol 162:1178–1194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichimura K, Casais C, Peck SC, Shinozaki K, Shirasu K (2006) MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J Biol Chem 281:36969–36976

    Article  CAS  PubMed  Google Scholar 

  • Jalmi SK, Sinha AK (2015) ROS mediated MAPK signaling in abiotic and biotic stress-striking similarities and differences. Front Plant Sci 6:769

    Article  PubMed  PubMed Central  Google Scholar 

  • Konishi M, Yanagisawa S (2010) Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response. Plant J 63:269–282

    Article  CAS  PubMed  Google Scholar 

  • Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M, Soyano T, Takahashi Y, Hirt H, Machida Y (2010) The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22:3778–3790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Křenek P, Niks RE, Vels A, Vyplelován P (2015) Genome-wide analysis of the barley MAPK gene family and its expression patterns in relation to Puccinia hordei infection. Acta Physiol Plant 37:254

    Article  Google Scholar 

  • Kumar K, Rao KP, Sharma P, Sinha AK (2008) Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiol Biochem 46:891–897

    Article  CAS  PubMed  Google Scholar 

  • Li SJ, Fu QT, Huang WD, Yu DQ (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep 28:683–693

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Zhu M, Hao L, Chen X, Gao Y, Guo X, Li H (2016) GhMAPKKK49, a novel cotton (Gossypium hirsutum L.) MAPKKK gene, is involved in diverse stress responses. Acta Physiol Plant 38:13

    Article  Google Scholar 

  • Merchant SS (2010) The elements of plant micronutrients. Plant Physiol 154:512–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meszaros T, Helfer A, Hatzimasoura E (2006) The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 48:485–498

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mishra NS, Tuteja R, Tuteja N (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452:55–68

    Article  CAS  PubMed  Google Scholar 

  • Moustafa K, AbuQamar S (2014) MAPK cascades and major abiotic stresses. Plant Cell Rep 33:1217–1225

    Article  CAS  PubMed  Google Scholar 

  • Nadarajah K, Sidek HM (2010) The green MAPKs. Asian J Plant Sci 9:1–10

    Article  CAS  Google Scholar 

  • Nakagami H, Kiegerl S, Hirt H (2004) OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 279:26959–26966

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trend Plant Sci 10:339–346

    Article  CAS  Google Scholar 

  • Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Bio Chem 281:38697–38704

    Article  CAS  Google Scholar 

  • Opdenakker K, Remans T, Vangronsveld J, Cuypers A (2012) Mitogen-activated protein (MAP) kinases in plant metal stress: regulation and responses in comparison to other biotic and abiotic stresses. Int J Mol Sci 13:7828–7853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009a) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Djamei A, Bitton F, Hirt H (2009b) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2:120–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren DT, Yang HP, Zhang SQ (2002) Cell death me diated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2009) 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 74:1–17

    Google Scholar 

  • Schünmann PHD, Richardson AE, Smith FW, Delhaize E (2004a) Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J Exp Bot 55:855–865

    Article  PubMed  Google Scholar 

  • Schünmann PHD, Richardson AE, Vickers CE, Delhaize E (2004b) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136:4205–4214

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Ding C, Li X, Xiao K (2012) Molecular characterization and expression analysis of TaZFP15, a C2H2- type zinc finger transcription factor gene in wheat (Triticum aestivum L.). J Integr Agric 11:31–42

    Article  CAS  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    Article  CAS  PubMed  Google Scholar 

  • Tena G, Asai T, Chiu WL, Sheen J (2001) Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 4:392–400

    Article  CAS  PubMed  Google Scholar 

  • Terauchi AM, Peers G, Kobayashi MC, Niyogi KK, Merchant SS (2010) Trophic status of Chlamy domonas reinhardtii influences the impact of iron deficiency on photosynthesis. Photosynth Res 105:39–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Zhang Y, Wang J, Wu X, Guo X (2007) MAP kinase gene in cotton (Gossypium hirsutum L.), GhMAPK, is involved in response to diverse environmental stresses. J Biochem Mol Biol 40:325–332

    CAS  PubMed  Google Scholar 

  • Wang JX, Ding HD, Zhang A, Ma FF, Cao JM, Jiang MY (2010) A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 52:442–452

    CAS  PubMed  Google Scholar 

  • Wang A, Jia C, Li J, Xu B, Jin Z (2015) Identifiacation of six mitogen-activated protein kinase (MAPK) genes in banana (Musa acuminate L. AAA group, cv. Cavendish) under infection of Fusarium Oxysporum f. sp. cubense Tropical Race 4. Acta Physiol Plant 37:115

    Article  Google Scholar 

  • 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. Plant Cell 15:745–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeh CM, Chien PS, Huang HJ (2007) Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58:659–671

    Article  CAS  PubMed  Google Scholar 

  • Yu S, Zhang L, Chen C, Li J, Ye S, Liu G, Mei X, Tang K, Luo L (2014) Isolation and characterization of BnMKK1 responsive to multiple stresses and affecting plant architecture in tobacco. Acta Physiol Plant 36:1313–1324

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the National Science Foundation of China (Grant No. 31671686), Natural Science Foundation of Hebei (Grant No. C2015204048), and the National Transgenic Major Program (Grant No. 2011ZX08008).

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Correspondence to Wenjing Lu or Kai Xiao.

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Communicated by J. Huang.

S. Yao and Y. Wang contributed equally to this work.

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Yao, S., Wang, Y., Yang, T. et al. Expression pattern and function of wheat mitogen-activated protein kinase (MPK) cascade genes under micronutrient-deprived conditions. Acta Physiol Plant 39, 40 (2017). https://doi.org/10.1007/s11738-016-2332-2

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