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BpTCP7 gene from Betula platyphylla regulates tolerance to salt and drought stress through multiple hormone pathways

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Abstract

TEOSINTE-LIKE1, CYCLOIDEA, and PROLIFERATING CELL FACTOR1 (TCP) genes are plant-specific transcription factors, which play important roles in plant growth and development. The function of CIN subclass of the TCP gene family has not been well revealed. In this investigation, five CIN subfamily members were identified in Betula platyphylla, all of which contained the conservative domains associated with the CIN subclass. Most of the genes were involved in the development of leaves, apical buds, and male inflorescences, especially the BpTCP7 gene. The results of GUS activity assays driven by BpTCP7 promoters confirmed these conclusions. The analysis of the BpTCP7 promoter also showed that the gene was induced by salt and drought stresses, and multiple hormones. Through Agrobacterium-mediated genetic transformation, we obtained four independent birch lines with over-expression of BpTCP7. Moreover, physiological and enzymatic analysis of transgenic lines under salt and drought stress showed that the scavenging effect of reactive oxygen species (ROS) of transgenic lines was improved. Our results provide useful information for revealing the functions of CIN subclasses in the growth and development of B. platyphylla and their applications in scavenging of ROS.

Key message

Overexpression of BpTCP7 gene leaded to improved scavenging reactive oxygen species (ROS) in drought and salinity treatment through multiple hormone pathways in Betula platyphylla.

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Abbreviations

TCP:

TEOSINTE-LIKE1, CYCLOIDEA, and PROLIFERATING CELL FACTOR1

CIN:

CINCINNATA

ROS:

Reactive oxygen species

qRT-PCR:

Quantificational real-time polymerase chain

SOD:

Superoxide dismutase

ORF:

Open reading frame

WPM:

Woody plant medium

References

  • Aguilar-Martinez JA, Poza-Carrion C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals with in axillary buds. Plant Cell 19:458–472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida DM, Gregorio GB, Oliveira MM, Saibo NJ (2017) Five novel transcription factors as potential regulators of OsNHX1 gene expression in a salt tolerant rice genotype. Plant Mol Biol 93(1–2):61–77

    CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Jiang BJ, Wu CX, Sun S, Hou WS, Han TF (2015) The characterization of GmTIP, a root-specific gene from soybean, and the expression analysis of its promoter. Plant Cell Tissue Organ Cult 121:259–274

    CAS  Google Scholar 

  • Classic Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    CAS  PubMed  Google Scholar 

  • Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk AD, Muino JM, Cutri L, Dornelas MC, Angenent GC, Immink RG (2012) Arabidopsis class I and class II TCP transcription factors regulate jasmonic acid metabolism and leaf development antagonistically. Plant Physiol 159(4):1511–1523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386(6624):485–488

    CAS  PubMed  Google Scholar 

  • Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20(9):2293–2306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Francis A, Dhaka N, Bakshi M, Jung KH, Sharma MK, Sharma R (2016) Comparative phylogenomic analysis provides insights into TCP gene functions in Sorghum. Sci Rep 6:38488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30(3):337–348

    CAS  PubMed  Google Scholar 

  • Koyama T, Furutani M, Tasaka M, Ohme-Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19(2):473–484

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama T, Mitsuda 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 22:3574–3588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kubota A, Ito S, Shim JS, Johnson RS, Song YH, Breton G, Goralogia GS, Kwon MS, Laboy Cintrón D, Koyama T, Ohme-Takagi M, Pruneda-Paz JL, Kay SA, MacCoss MJ, Imaizumi T (2017) TCP4-dependent induction of CONSTANS transcription requires GIGANTEA in photoperiodic flowering in Arabidopsis. PLoS Genet 13(6):e1006856

    PubMed  PubMed Central  Google Scholar 

  • Lescot M, Dehais 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 30:325–327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Zachgo S (2013) TCP3 interacts with R2R3-MYB proteins,promotes flavonoid biosynthesis and negatively regulates the auxin response in Arabidopsis thaliana. Plant J 76(6):901–913

    CAS  PubMed  Google Scholar 

  • Li HY, Jiang J, Wang S, Liu FF (2010a) Expression analysis of ThGLP, a new germin-like protein gene, in Tamarix hispida. J For Res 21(3):323–330

    CAS  Google Scholar 

  • Li QF, Sun SM, Yuan DY, Yu HX, Gu MH, Liu QQ (2010b) Validation of candidate reference genes for the accurate normalization of real-time quantitative RT-PCR data in rice during seed development. Plant Mol Biol Rep 28:49–57

    Google Scholar 

  • Li Z, Li B, Shen WH, Huang H, Dong A (2012) TCP transcription factors interact with AS2 in the repression of class-I KNOX genes in Arabidopsis thaliana. Plant J 71(1):99–107

    CAS  PubMed  Google Scholar 

  • Liu BX, Wang ZG, Liang HY, Yang MS (2012) Effects of salt stress on physiological characters and salt-tolerance of Ulmus pumila in different habitats. Chin J Appl Ecol 23(6):1481–1489

    CAS  Google Scholar 

  • Martin-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39

    CAS  PubMed  Google Scholar 

  • Masuda HP, Cabral LM, De Veylder L, Tanurdzic M, de Almeida Engler J, Geelen D, Inzé D, Martienssen RA, Ferreira PC, Hemerly AS (2008) ABAP1 is a novel plant Armadillo BTB protein involved in DNA replication and transcription. EMBO J 27(20):2746–2756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay P, Tyagi AK (2015) OsTCP19 influences developmental and abiotic stress signaling by modulating ABI4-mediated pathways. Sci Rep 5:9998

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nath U, Aggarwal P, Challa KR (2016) Activation of YUCCA5 by the transcription factor TCP4 integrates developmental and environmental signals to promote hypocotyl elongation in Arabidopsis. Plant Cell 28:2117–2130

    PubMed  PubMed Central  Google Scholar 

  • Navaud O, Dabos P, Carnus E, Tremousaygue D, Hervé C (2007) TCP transcription factors predate the emergence of land plants. J Mol Evol 65(1):23–33

    CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263

    CAS  PubMed  Google Scholar 

  • Parapunova V, Busscher M, Busscher-Lange J, Lammers M, Karlova R, Bovy AG (2014) Identification, cloning and characterization of the tomato TCP transcription factor family. BMC Plant Biol 14:157

    PubMed  PubMed Central  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants. Ecotoxicol Environ Safe 60:324–349

    CAS  PubMed  Google Scholar 

  • Sarvepalli K, Nath U (2011) Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J 67:595–607

    CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3(6):1101–1108

    CAS  PubMed  Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6(9):e230

    PubMed  PubMed Central  Google Scholar 

  • Shleizer-Burko S, Burko Y, Ben-Herzel O, Ori N (2011) Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning. Development 138(4):695–704

    CAS  PubMed  Google Scholar 

  • Tao J, Zhan YG, Jiang J, Yang CP, Liu YX (1998) Tissue culture and regenerative system of Betula platyphylla Suks. J Northeast For Univ 26(5):6–9

    Google Scholar 

  • Tao Q, Guo D, Wei B, Zhang F, Pang C, Jiang H, Zhang J, Wei T, Gu H, Qu LJ, Qin G (2013) The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell 25(2):421–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vadde BVL, Challa KR, Nath U (2018) The TCP4 transcription factor regulates trichome cell differentiation by directly activating GLABROUS INFLORESCENCE STEMS in Arabidopsis thaliana. Plant J 93(2):259–269

    CAS  PubMed  Google Scholar 

  • Wang DM, Jia Y, Cui JZ (2009) Advances in research on effects of salt stress on plant and adaptive mechanism of the plant to salinity. Chin Agric Sci Bull 25(04):124–128

    Google Scholar 

  • Wang ST, Sun XL, Hoshino Y, Yu Y, Jia B, Sun ZW, Sun MZ, Duan XB, Zhu YM (2014a) MicroRNA319 positively regulates cold tolerance by targeting OsPCF and OsTCP21 in rice (Oryza sativa L.). PLoS ONE 9(3):e91357

    PubMed  PubMed Central  Google Scholar 

  • Wang X, Jiang Q, Wang W, Su L, Han Y, Wang C (2014b) Molecular mechanism of polypeptides from Chlamys farreri (PCF)'s anti-apoptotic effect in UVA-exposed HaCaT cells involves HSF1/HSP70, JNK, XO, iNOS and NO/ROS. J Photochem Photobiol B 130:47–56

    CAS  PubMed  Google Scholar 

  • Xu R, Sun P, Jia F, Lu L, Li Y, Zhang S (2014) Genome wide analysis of TCP transcription factor gene family in Malus domestica. Genetics 93:733–746

    CAS  Google Scholar 

  • Yang G, Chen S, Wang S, Liu GF, Li HY, Huang HJ, Jiang J (2015) BpGH3.5, an early auxin-response gene, regulates root elongation in Betula platyphylla × Betula pendula. Plant Cell Tissue Org 120(1):239–250

    CAS  Google Scholar 

  • Zhan YG, Liu ZH, Wang YC, Wang ZY, Yang CP, Liu GF (2001) Transformation of insect resistant gene into birch. J Northeast For Univ 29(6):4–6

    CAS  Google Scholar 

  • Zhou M, Li D, Li Z, Hu Q, Yang C, Zhu L, Luo H (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 161(3):1375–1391

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Fundamental Research Funds for the Central Universities (No. 2572018BW03), the Innovation Project of State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University) (2015B01), the 111 Project (B16010), Provincial Funding for Major National Science and Technology Projects and Key R&D Projects in Heilongjiang Province (GX18B027).

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Author notes

  1. Huiyu Li and Hongmei Yuan contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China

    Huiyu Li, Jiayu Luan, Yang Yang, Li Ren, Linjun An & Jing Jiang

  2. Heilongjiang Academy of Agricultural Sciences Postdoctoral Programme, 368 Xuefu Road, Harbin, 150086, China

    Hongmei Yuan

  3. The Experimental Centre of Tropical Forestry, Chinese Academy of Forestry, Pingxiang, 532600, China

    Fumei Liu

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  1. Huiyu Li
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  2. Hongmei Yuan
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  6. Li Ren
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  7. Linjun An
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Contributions

JJ designed and managed the research work and improved the manuscript; HL designed the research work and wrote the manuscript; HY wrote the manuscript; LA performed the bioinformatics analysis; FM, YY and JL performed the experiments; LR prepared all figures. All the authors reviewed the manuscript.

Corresponding author

Correspondence to Jing Jiang.

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Communicated by Sergio J. Ochatt.

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Li, H., Yuan, H., Liu, F. et al. BpTCP7 gene from Betula platyphylla regulates tolerance to salt and drought stress through multiple hormone pathways. Plant Cell Tiss Organ Cult 141, 17–30 (2020). https://doi.org/10.1007/s11240-019-01748-7

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  • DOI: https://doi.org/10.1007/s11240-019-01748-7

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