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Characterization and primary functional analysis of a bamboo NAC gene targeted by miR164b

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Abstract

Key message

PeSNAC1 , a stress-related NAC1 from Phyllostachys edulis , was characterized. Ectopic expression in Arabidopsis indicated that PeSNAC1 together with ped -miR164b participated in the regulation of organ boundaries and stress tolerance.

Abstract

NAC (NAM, ATAF1/2 and CUC2) participates in many different processes regulating plant growth, development, and stress response. A total of 125 NAC genes have been predicted in moso bamboo (Phyllostachys edulis), but their roles are poorly understood. PeSNAC1 targeted by ped-miR164b was focused for further study. The cleavage of PeSNAC1 mRNA guided by ped-miR164b was validated using RLM-5′ RACE. Tissue-specific expression analysis demonstrated that ped-miR164b had a declining trend from root, sheath, leaf, to that of stem, which was opposite to that of PeSNAC1. Transgenic Arabidopsis plants overexpressing either PeSNAC1 (OX-PeSNAC1) or, ped-miR164b (OX-ped-miR164b) driven by the CaMV35S promoter were generated. OX-ped-miR164b plants showed similar phenotype of cuc2 mutants whose growth was seriously suppressed. Compared with Col-0, sense OX-PeSNAC1 plants grew rapidly and flowered earlier, whereas antisense plants grew slowly and exhibited delayed flowering. Sense OX-PeSNAC1 plants had the greatest number of lateral roots, while antisense OX-PeSNAC1 and OX-ped-miR164b plants had fewer lateral roots than Col-0. Under NaCl and PEG6000 stresses, survival rates were higher and F v/F m values declined more slowly in sense OX-PeSNAC1 plants than in Col-0, with lower survival rates and a more rapid decrease in F v/F m values conversely observed in antisense OX-PeSNAC1 and OX-ped-miR164b plants. These findings indicated that ped-miR164b-targeted PeSNAC1 may play key roles in plant development and tolerance to salinity and drought stresses.

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Abbreviations

ATAF:

Arabidopsis transcription activation factor

BLAST:

Basic local alignment search tool

CaMV35S :

Cauliflower mosaic virus 35S

cDNA:

Complementary DNA

F v/F m :

Maximal quantum yield of PSII

ORF:

Open reading frame

CUC:

Cup-shaped cotyledon (CUC), a NAC protein

miRNA:

MicroRNA, small regulatory RNAs

NAC:

Abbreviation of NAM, ATAF1/2 and CUC2, a plant-specific TF family

NAM:

No apical meristem (NAM), a NAC protein

PCR:

Polymerase chain reaction

qPCR:

Real time quantitative PCR

RACE:

Rapid-amplification of cDNA ends

RLM-5′ RACE:

RNA ligase-mediated 5′ RACE

TF:

Transcription factor

References

  • Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15(12):664–674

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler K (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179

    Article  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  CAS  PubMed  Google Scholar 

  • Cui K, He CY, Zhang JG, Duan AG, Zeng YF (2012) Temporal and spatial profiling of internode elongation-associated protein expression in rapidly growing culms of bamboo. J Proteome Res 11(4):2492–2507

    Article  CAS  PubMed  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39(Web Server issue):W155–W159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demmig-Adams B, Adams WWI (1996) Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field. Aust J Plant Physiol 23(5):649–659

    Article  CAS  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62(10):3563–3573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan C, Ma J, Guo Q, Li X, Wang H, Lu M (2013) Selection of reference genes for quantitative real-time PCR in bamboo (Phyllostachys edulis). PLoS One 8(2):e56573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang Y, Xie K, Xiong L (2014) Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. J Exp Bot 65(8):2119–2135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao ZM, Fan SH, Gao J, Li XP, Cai CJ, Peng ZH (2006) Extract genomic DNA from Phyllostachys edulis by CTAB-based method. For Res 19(6):725–728 (in Chinese)

    Google Scholar 

  • Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL (2008) The Vienna RNA websuite. Nucleic Acids Res 36(Web Server issue):W70–W74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down regulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He CY, Cui K, Zhang JG, Duan AG, Zeng YF (2013) Next-generation sequencing-based mRNA and microRNA expression profiling analysis revealed pathways involved in the rapid growth of developing culms in Moso bamboo. BMC Plant Biol 13:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18(11):2946–2957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang Q, Wang Y, Li B, Chang J, Chen M, Li K, Yang G, He G (2015) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol 15:268

    Article  PubMed  PubMed Central  Google Scholar 

  • Jefferson RA (1987) Assaying for chimeric genes in plants: the GUS fusion system. Plant Mol Biol Rep 5(4):387–405

    Article  CAS  Google Scholar 

  • Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23(12):4185–4207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131(17):4311–4322

    Article  CAS  PubMed  Google Scholar 

  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18(4):263–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Guo G, Guo W, Guo G, Tong D, Ni Z, Sun Q, Yao Y (2012) MiRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Hu S, Cao Y, Xu G (2015) Bioinformatics analysis of NAC gene family in moso bamboo. Genomics Appl Biol 34(8):1769–1777 (in Chinese)

    Google Scholar 

  • Lin R, Zhao W, Meng X, Wang M, Peng Y (2007) Rice gene OsNAC19 encodes anovel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci 172(1):120–130

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14(12):1035–1046

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence–a practical guide. J Exp Bot 51(345):659–668

    Article  CAS  PubMed  Google Scholar 

  • Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell Physiol 36(8):1405–1420

    CAS  PubMed  Google Scholar 

  • Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2010) Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61:165–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465(1–2):30–44

    Article  CAS  PubMed  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “Redox” and abscisic acid-mediated controls. Plant Physiol 129(2):460–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Z, Lu Y, Li L, Zhao Q, Feng Q, Gao Z, Lu H, Hu T, Yao N, Liu K, Li Y, Fan D, Guo Y, Li W, Lu Y, Weng Q, Zhou C, Zhang L, Huang T, Zhao Y, Zhu C, Liu X, Yang X, Wang T, Miao K, Zhuang C, Cao X, Tang W, Liu G, Liu Y, Chen J, Liu Z, Yuan L, Liu Z, Huang X, Lu T, Fei B, Ning Z, Han B, Jiang Z (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45(4):456–461

    Article  CAS  PubMed  Google Scholar 

  • Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55(1):65–76

    Article  CAS  PubMed  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520

    Article  CAS  PubMed  Google Scholar 

  • Shen H, Yin YB, Chen F, Xu Y, Dixon RA (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenergy Res 2:217–232

    Article  Google Scholar 

  • Song JB, Gao S, Sun D, Li H, Shu XX, Yang ZM (2013) miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. BMC Plant Biol 13:210

    Article  PubMed  PubMed Central  Google Scholar 

  • Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) The No Apical Meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85(2):159–170

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Koyama T, Mistuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22(11):3574–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unver T, Budak H (2009) Conserved microRNAs and their targets in model grass species Brachypodium distachyon. Planta 230(4):659–669

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Zheng Y, Xin H, Fang L, Li S (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32(1):61–75

    Article  PubMed  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14(23):024–3036

    CAS  Google Scholar 

  • Xu P, Mohorianu I, Yang L, Zhao H, Gao Z, Dalmay T (2014) Small RNA profile in moso bamboo root and leaf obtained by high definition adapters. PLoS ONE 9(7):e103590

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang L, Lou Y, Peng Z, Zhao H, Sun H, Gao Z (2015) Molecular characterization and primary functional analysis of PeMPEC, a magnesium-protoporphyrin IX monomethyl ester cyclase gene of bamboo (Phyllostachys edulis). Plant Cell Rep 34(11):2001–2011

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8(6):R96

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Chen D, Peng Z, Wang L, Gao Z (2013) Identification and characterization of microRNAs in the leaf of ma bamboo (Dendrocalamus latiflorus) by deep sequencing. PLoS One 8(10):e78755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Peng Z, Fei B, Li L, Hu T, Gao Z, Jiang Z (2014a) BambooGDB: a bamboo genome database with functional annotation and an analysis platform. Database (Oxford) 2014:bau006

    Article  Google Scholar 

  • Zhao H, Wang L, Dong L, Sun H, Gao Z (2014b) Discovery and comparative profiling of microRNAs in representative monopodial bamboo (Phyllostachys edulis) and sympodial bamboo (Dendrocalamus latiflorus). PLoS One 9(7):e102375

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu G, Chen G, Zhu J, Zhu Y, Lu X, Li X, Hu Y, Yan Y (2015) Molecular characterization and expression profiling of NAC transcription factors in Brachypodium distachyon L. PLoS One 10(10):e0139794

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work received financial support from the Special Fund for Forest Scientific Research in the Public Welfare from State Forestry Administration of China (No. 201504106) and the Sub-Project of National Science and Technology Support Plan of the Twelfth Five-Year in China (No. 2015BAD04B01 and No. 2015BAD04B03).

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Correspondence to Zhimin Gao.

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Communicated by B. Li.

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Wang, L., Zhao, H., Chen, D. et al. Characterization and primary functional analysis of a bamboo NAC gene targeted by miR164b. Plant Cell Rep 35, 1371–1383 (2016). https://doi.org/10.1007/s00299-016-1970-6

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