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Arabidopsis root apical meristem survival during waterlogging is determined by phytoglobin through nitric oxide and auxin

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Abstract

Main conclusion

Over-expression of phytoglobin mitigates the degradation of the root apical meristem (RAM) caused by waterlogging through changes in nitric oxide and auxin distribution at the root tip.

Abstract

Plant performance to waterlogging is ameliorated by the over-expression of the Arabidopsis Phytoglobin 1 (Pgb1) which also contributes to the maintenance of a functional RAM. Hypoxia induces accumulation of ROS and damage in roots of wild type plants; these events were preceded by the exhaustion of the RAM resulting from the loss of functionality of the WOX5-expressing quiescent cells (QCs). These phenotypic deviations were exacerbated by suppression of Pgb1 and attenuated when the same gene was up-regulated. Genetic and pharmacological studies demonstrated that degradation of the RAM in hypoxic roots is attributed to a reduction in the auxin maximum at the root tip, necessary for the specification of the QC. This reduction was primarily caused by alterations in PIN-mediated auxin flow but not auxin synthesis. The expression and localization patterns of several PINs, including PIN1, 2, 3 and 4, facilitating the basipetal translocation of auxin and its distribution at the root tip, were altered in hypoxic WT and Pgb1-suppressing roots but mostly unchanged in those over-expressing Pgb1. Disruption of PIN1 and PIN2 signal in hypoxic roots suppressing Pgb1 initiated in the transition zone at 12 h and was specifically associated to the absence of Pgb1 protein in the same region. Exogenous auxin restored a functional RAM, while inhibition of the directional auxin flow exacerbated the degradation of the RAM. The regulation of root behavior by Pgb1 was mediated by nitric oxide (NO) in a model consistent with the recognized function of Pgbs as NO scavengers. Collectively, this study contributes to our understanding of the role of Pgbs in preserving root meristem function and QC niche during conditions of stress, and suggests that the root transition zone is most vulnerable to hypoxia.

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All materials and data used or generated in this study can be made available upon request.

Abbreviations

NAA:

Auxin 1-naphtaleneacetic acid

NPA:

Naphthaleneacetic acid acid

Pgb:

Phytoglobin

QC:

Quiescent cells

RAM:

Root apical meristem

SNP:

Sodium nitroprusside

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Acknowledgements

The authors thank the following colleagues for providing the Arabidopsis lines: Dr. Hebelstrup (35S:Pgb1 and Pgb1–RNAi); and Dr. Lorenzo (PIN–GFP).

Funding

This work was supported by a NSERC Discovery Grant to CS and a NSERC CRD Grant to RWD and CS.

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Authors and Affiliations

  1. Department of Plant Science, University of Manitoba, Winnipeg, MB, R3T 2N2, Canada

    Mohammed M. Mira, Eman A. El-Khateeb, Mohamed S. Youssef, Kenny So, Robert W. Duncan, Robert D. Hill & Claudio Stasolla

  2. Department of Botany, Faculty of Science, Tanta University, Tanta, 31527, Egypt

    Mohammed M. Mira & Eman A. El-Khateeb

  3. Department of Botany and Microbiology, Faculty of Science, Kafrelsheikh University, Kafrelsheikh, 33516, Egypt

    Mohamed S. Youssef

  4. Department of Plant Physiology, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776, Warsaw, Poland

    Katarzyna Ciacka

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Contributions

MMM performed the majority of the experiments and helped writing the manuscript. EAE did the waterlogging experiments and some of the immunolocalization analyses. MSY helped with the waterlogging experiments and the phenotypic characterization of the lines. KC helped with some of the gene expression studies. KS optimized the antibody analyses. RWD contributed with the antibody analyses and funded some of the experiments. RDW contributed with the interpretation of data and writing. CS conceptualized the work, interpreted the data, and helped with the writing.

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Correspondence to Claudio Stasolla.

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Mira, M.M., El-Khateeb, E.A., Youssef, M.S. et al. Arabidopsis root apical meristem survival during waterlogging is determined by phytoglobin through nitric oxide and auxin. Planta 258, 86 (2023). https://doi.org/10.1007/s00425-023-04239-4

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