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Comparative spatiotemporal analysis of root aerenchyma formation processes in maize due to sulphate, nitrate or phosphate deprivation

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Abstract

Nitrate (N), phosphate (P) or sulphate (S) deprivation causes aerenchyma formation in maize (Zea mays L.) nodal roots. The exact mechanisms that trigger the formation of aerenchyma under these circumstances are unclear. We have compared aerenchyma distribution across the nodal roots of first whorl (just emerging in 10-day-old seedlings), which were subject to S, N or P deprivation over a period of 10 days in connection with oxygen consumption, ATP concentration, cellulase and polygalacturonase activity in the whole root. The effect of deprivation on aerenchyma formation was examined using light and electron microscopy, along with in situ detection of calcium and of reactive oxygen species (ROS) by fluorescence microscopy. Aerenchyma was not found in the root base regardless of the deprivation. Programmed cell death (PCD) was observed near the root tip, either within the first two days (−N) or a few days later (−S, −P) of the treatment. Roots at day 6 under all three nutrient-deprived conditions showed signs of PCD 1 cm behind the cap, whereas only N-deprived root cells 0.5 cm behind the cap showed severe ultrastructural alterations, due to advanced PCD. The lower ATP concentration and the higher oxygen consumptions observed at day 2 in N-, P- and S-deprived roots compared to the control indicated that PCD may be triggered by perturbations in energy status of the root. The peaks of cellulase activity located between days 3 (−N) and 6 (−P), along with the respective alterations in polygalacturonase activity, indicated a coordination which preceded aerenchyma formation. ROS and calcium seemed to contribute to PCD initiation, with ROS possessing dual roles as signals and eliminators. All the examined parameters presented both common features and characteristic variations among the deprivations.

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Abbreviations

PCD:

Programmed cell death

NOX:

NADPH oxidase

MPT:

Mitochondrial permeability transition

nPCD:

Nutritional programmed cell death

ROS:

Reactive oxygen species

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Acknowledgements

We would like to express our appreciation to Syngenta Hellas and G. Pontikas for the supply of maize seeds. We also wish to thank the reviewers for their useful comments. This research work was additionally supported by the Austrian Science Fund (FWF P18976). Rothamsted Research receives grant-aided support from the UK's Biotechnology and Biological Sciences Research Council.

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The authors declare that they have no conflict of interest.

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Correspondence to Dimitris L. Bouranis.

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Siyiannis, V.F., Protonotarios, V.E., Zechmann, B. et al. Comparative spatiotemporal analysis of root aerenchyma formation processes in maize due to sulphate, nitrate or phosphate deprivation. Protoplasma 249, 671–686 (2012). https://doi.org/10.1007/s00709-011-0309-y

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