Journal of Plant Biology

, Volume 61, Issue 6, pp 366–373 | Cite as

A NAC Transcription Factor ZmNAC84 affects Pollen Development Through the Repression of ZmRbohH Expression in Maize

  • Qi Yang
  • Heping Zhang
  • Chen Liu
  • Liping Huang
  • Lili Zhao
  • Aying Zhang
Original Article


The NAC proteins are plant-specific transcription factors and widely distributed in plants. The wide functions of NAC transcription factors were studied, but the roles of NAC in pollen development are largely unclear. Here, we found that ZmNAC84 played a vital role in maize pollen development. ZmRbohH showed high expression in pollen. ZmNAC84 inhibited the ZmRbohH expression by directly binding to its promoter in pollen. Moreover, phosphorylation of ZmNAC84 at Ser113 played an important role in this process. These results suggest that ZmNAC84 plays a negative role in pollen development possibly via repressing the ZmRbohH expression.


Pollen development Zea mays ZmNAC84 ZmRbohH 


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  1. Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, Yaeno T, Shirasu K, Yoshioka H (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27:2645–2663CrossRefGoogle Scholar
  2. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857CrossRefGoogle Scholar
  3. Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor M, Xue GP (2011) Mueller-Roeber, B. ORS1, an H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4:346–360Google Scholar
  4. Chang YL, Li WY, Miao H, Yang SQ, Li R, Wang X, Li WQ, Chen KM (2016) Comprehensive genomic analysis and expression profiling of the NOX gene families under abiotic stresses and hormones in plants. Genome Biol Evol 8:791–810CrossRefGoogle Scholar
  5. Chen SP, Lin IW, Chen XY, Huang YH, Chang SC, Lo HS, Lu HH, Yeh KW (2016) Sweet potato NAC transcription factor, IbNAC1, upregulates sporamin gene expression by binding the SWRE motif against mechanical wounding and herbivore attack. Plant J 86:234–248CrossRefGoogle Scholar
  6. Cui J, You CJ, Zhu EG, Huang Q, Ma H, Chang F (2016) Feedback regulation of DYT1 by interactions with downstream bHLH factors promotes DYT1 nuclear localization and anther development. Plant Cell 28:1078–1093CrossRefGoogle Scholar
  7. Ernst HA, Olsen AN, Skriver K, Larsen S, Leggio LL (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303CrossRefGoogle Scholar
  8. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Takagi MO, Tran LSP, Shinozaki KY, Shinozaki K (2004) A dehydrationinduced NAC protein, RD26, is involved in a novel ABAdependent stress-signaling pathway. Plant J 39:863–876CrossRefGoogle Scholar
  9. Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313CrossRefGoogle Scholar
  10. He H, Yan JW, Yu XY, Liang Y, Fang L, Scheller HV, Zhang AY (2017) The NADPH-oxidase AtRbohl plays a positive role in drought-stress response in Arabidopsis thaliana. Biochem Bioph Res Co 491:834–839CrossRefGoogle Scholar
  11. Hord CLH, Sun YJ, Pillitteri LJ, Torii KU, Wang HC, Zhang SQ, Ma H (2008) Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol Plant 1:645–658CrossRefGoogle Scholar
  12. Huang LP, Jia J, Zhao XX, Zhang MY, Huang XX, Ji E, Ni L, Jiang MY (2018a) The ascorbate peroxidase APX1 is a direct target of a zinc finger transcription factor ZFP36 and a late embryogenesis abundant protein OsLEA5 interacts with ZFP36 to co-regulate OsAPX1 in seed germination in rice. Biochem Bioph Res Co 495:339–345CrossRefGoogle Scholar
  13. Huang LP, Zhang MY, Jia J, Zhao XX, Huang XX, Ji E, Ni L, Jiang MY (2018b) An atypical late embryogenesis abundant protein OsLEA5 plays a positive role in ABA-induced antioxidant defense In Oryza Sativa L. Plant Cell Physiol 59:916–929CrossRefGoogle Scholar
  14. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907CrossRefGoogle Scholar
  15. Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080CrossRefGoogle Scholar
  16. Kim MJ, Park MJ, Seo PJ, Song JS, Kim HJ, Park CM (2012) Controlled nuclear import of the transcription factor NTL6 reveals a cytoplasmic role of SnRK2.8 in the drought-stress response. Biochem J 448:353–363CrossRefGoogle Scholar
  17. Kim YS, Sakuraba Y, Han SH, Yoo SC, Paek NC (2013) Mutation of the Arabidopsis NAC016 Transcription Factor Delays Leaf Senescence. Plant Cell Physiol 54:1660–1672CrossRefGoogle Scholar
  18. Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844CrossRefGoogle Scholar
  19. Li WT, Zhu ZW, Chern M, Yin JJ, Yang C, Ran L, Cheng MP, He M, Wang K, Wang J, Zhou XG, Zhu XB, Chen ZX, Wang JC, Zhao W, Ma BT, Qin P, Chen WL, Wang YP, Liu JL, Wang WM, Wu XJ, Li P, Wang JR, Zhu LH, Li SG, Chen XW (2017) A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170:114–126CrossRefGoogle Scholar
  20. Mao CJ, Lu SC, Lv B, Zhang B, Shen JB, He JM, Luo LQ, Xi DD, Chen X, Ming F (2017) A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiol 174:1747–1763.CrossRefGoogle Scholar
  21. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15CrossRefGoogle Scholar
  22. Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006CrossRefGoogle Scholar
  23. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326CrossRefGoogle Scholar
  24. Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751CrossRefGoogle Scholar
  25. Potocký M, Pejchar P, Gutkowska M, Jiménez-Quesada MJ, Potocká A, Alché JD, Kost B, Žárský V (2012) NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. J Plant Physiol 169:1654–1663CrossRefGoogle Scholar
  26. Sakuraba Y, Kim YS, Han SH, Lee BD, Peak NC (2015) The Arabidopsis transcription factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell 27:1771–1787CrossRefGoogle Scholar
  27. Seo PJ, Park CM (2010) A membrane-bound NAC transcription factor as an integrator of biotic and abiotic stress signals. Plant Signal Behav 5:481–483CrossRefGoogle Scholar
  28. Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131:1491–1501CrossRefGoogle Scholar
  29. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699CrossRefGoogle Scholar
  30. Tian HN, Wang XL, Guo HY, Cheng YX, Hou CJ, Chen JG, Wang SC (2017) NTL8 regulates trichome formation in Arabidopsis by directly activating R3 MYB genes TRY and TCL1. Plant Physiol 174:2363–2375CrossRefGoogle Scholar
  31. Tran LSP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a droughtresponsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498CrossRefGoogle Scholar
  32. Wang Z, Li J, Chen SX, Heng YF, Chen Z, Yang J (2017) Zhou, K.J.; Pei, J.W.; He, H.; Deng, X.W.; Ma, L.G. Poaceae-specific &ITMS1&IT encodes a phospholipid-binding protein for male fertility in bread wheat. Proc Natl Acad Sci USA 114:12614–12619Google Scholar
  33. Wu H, Fu B, Sun PP, Xiao C, Liu JH (2016) A NAC transcription factor represses putrescine biosynthesis and affects drought tolerance. Plant Physiol 172:1532–1547CrossRefGoogle Scholar
  34. Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Gene Dev 14:3024–3036CrossRefGoogle Scholar
  35. Zhang H, Liu YP, Wen F, Yao DM, Wang L, Guo J, Ni L, Zhang AY, Tan MP, Jiang MY (2014) A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. J Exp Bot 65:5795–5809CrossRefGoogle Scholar
  36. Zhu E, You CJ, Wang SS, Cui J, Niu BX, Wang YX, Qi J, Ma H, Chang F (2015) The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J 83:976–990CrossRefGoogle Scholar
  37. Zhu Y, Yan JW, Liu WJ, Liu L, Sheng Y, Sun Y, Li YY, Scheller HV, Jiang MY, Hou XL, Ni L, Zhan AY (2016) Phosphorylation of a NAC transcription factor by a Calcium/Calmodulin-dependent protein kinase regulates abscisic acid-induced antioxidant defense in Maize. Plant Physiol 171:1651–1664CrossRefGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Qi Yang
    • 1
  • Heping Zhang
    • 1
  • Chen Liu
    • 1
  • Liping Huang
    • 1
    • 2
  • Lili Zhao
    • 1
  • Aying Zhang
    • 1
  1. 1.National Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Life SciencesNanjing Agricultural UniversityNanjingPR China
  2. 2.Department of Horticulture, School of Food Science and EngineeringFoshan UniversityFoshanPR China

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