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The wheat TabZIP2 transcription factor is activated by the nutrient starvation-responsive SnRK3/CIPK protein kinase

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Abstract

Key message

The understanding of roles of bZIP factors in biological processes during plant development and under abiotic stresses requires the detailed mechanistic knowledge of behaviour of TFs.

Abstract

Basic leucine zipper (bZIP) transcription factors (TFs) play key roles in the regulation of grain development and plant responses to abiotic stresses. We investigated the role and molecular mechanisms of function of the TabZIP2 gene isolated from drought-stressed wheat plants. Molecular characterisation of TabZIP2 and derived protein included analyses of gene expression and its target promoter, and the influence of interacting partners on the target promoter activation. Two interacting partners of TabZIP2, the 14-3-3 protein, TaWIN1 and the bZIP transcription factor TaABI5L, were identified in a Y2H screen. We established that under elevated ABA levels the activity of TabZIP2 was negatively regulated by the TaWIN1 protein and positively regulated by the SnRK3/CIPK protein kinase WPK4, reported previously to be responsive to nutrient starvation. The physical interaction between the TaWIN1 and the WPK4 was detected. We also compared the influence of homo- and hetero-dimerisation of TabZIP2 and TaABI5L on DNA binding. TabZIP2 gene functional analyses were performed using drought-inducible overexpression of TabZIP2 in transgenic wheat. Transgenic plants grown under moderate drought during flowering, were smaller than control plants, and had fewer spikes and seeds per plant. However, a single seed weight was increased compared to single seed weights of control plants in three of four evaluated transgenic lines. The observed phenotypes of transgenic plants and the regulation of TabZIP2 activity by nutrient starvation-responsive WPK4, suggest that the TabZIP2 could be the part of a signalling pathway, which controls the rearrangement of carbohydrate and nutrient flows in plant organs in response to drought.

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Abbreviations

3D:

Three-dimensional

ABA:

Abscisic acid

COR:

Cold responsive

DOPE:

Discrete optimised protein energy

DHN:

Dehydrin

GFP:

Green fluorescent protein

HD-Zip I:

Homeodomain-leucine zipper class I

IWGSC:

International Wheat Genome Sequencing Consortium

LEA:

Late embryogenesis abundant

MOF:

Modeller objective function

Q-PCR:

Quantitative RT-PCR

Ta:

Triticum aestivum

TF(s):

Transcription factor(s)

Y1H:

Yeast-1-hybrid

Y2H:

Yeast-2-hybrid

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Acknowledgements

The plant transformation contribution of Ainur Ismagul is acknowledged. We also thank Ursula Langridge, Larissa Chirkova and Yagnesh Nagarajan for technical assistance, and Julie Hayes and Carl Simmons for critically reading the manuscript. Pradeep K. Agarwal is grateful to the Council of Scientific and Industrial Research of India (Raman Research Fellowship) and Syed Sarfraz Hussain to DuPont Pioneer for funding their fellowships. This work was supported by the Australian Research Council (LP120100201 to MH and SL), the Australian Grains Research and Development Corporation, the Government of South Australia, and DuPont Pioneer, as part of LP120100201.

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Author notes

  1. Sukanya Luang

    Present address: Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand

  2. Natalia Bazanova

    Present address: Commonwealth Scientific and Industrial Research Organisation, Glen Osmond, SA, 5064, Australia

  3. Omid Eini

    Present address: Department of Plant Protection, School of Agriculture, University of Zanjan, Zanjan, Iran

  4. Syed Sarfraz Hussain

    Present address: Forman Christian College, Lahore, 54600, Pakistan

  5. Sukanya Luang and Pradeep Sornaraj have contributed equally to this work.

Authors and Affiliations

  1. School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, SA, 5064, Australia

    Sukanya Luang, Pradeep Sornaraj, Natalia Bazanova, Wei Jia, Omid Eini, Syed Sarfraz Hussain, Nataliya Kovalchuk, Maria Hrmova & Sergiy Lopato

  2. CSIR-Central Salt and Marine Chemicals Research Institute, Gijubhai Badheka Marg, Bhavnagar, India

    Pradeep K. Agarwal

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  3. Natalia Bazanova
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  4. Wei Jia
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  9. Maria Hrmova
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Contributions

Conceived, designed experiments and analysed data: SLu, PS, MH and SLo. Plant growth and transformation: PS, NK, OE and PKA. Cloning, Y1H, pull-down and transient expression assays, Q-PCR experiments: WJ, NBa and SLo. Protein–protein interactions: SH and MH. 3D molecular modelling: SLu and MH. Discussed the data and contributed to writing: SLu and PS. Writing of the manuscript: SLo and MH.

Corresponding author

Correspondence to Maria Hrmova.

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Authors declare that they have no conflict of interest.

Additional information

GeneBank accession numbers

TabZIP2 (KT224373), WPK4 (AB011670), TaABI5L (MF034144), and TaWIN1 (MF034145).

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Supplementary material 1 (DOCX 105 KB)

Supplementary material 2 (PDF 5501 KB)

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Luang, S., Sornaraj, P., Bazanova, N. et al. The wheat TabZIP2 transcription factor is activated by the nutrient starvation-responsive SnRK3/CIPK protein kinase. Plant Mol Biol 96, 543–561 (2018). https://doi.org/10.1007/s11103-018-0713-1

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  • DOI: https://doi.org/10.1007/s11103-018-0713-1

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