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Effect of ancymidol on cell wall metabolism in growing maize cells

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Abstract

Main conclusion

Ancymidol inhibits the incorporation of cellulose into cell walls of maize cell cultures in a gibberellin-independent manner, impairing cell growth; the reduction in the cellulose content is compensated with xylans.

Ancymidol is a plant growth retardant which impairs gibberellin biosynthesis. It has been reported to inhibit cellulose synthesis by tobacco cells, based on its cell-malforming effects. To ascertain the putative role of ancymidol as a cellulose biosynthesis inhibitor, we conducted a biochemical study of its effect on cell growth and cell wall metabolism in maize cultured cells. Ancymidol concentrations ≤ 500 µM progressively reduced cell growth and induced globular cell shape without affecting cell viability. However, cell growth and viability were strongly reduced by ancymidol concentrations ≥ 1.5 mM. The I50 value for the effect of ancymidol on FW gain was 658 µM. A reversal of the inhibitory effects on cell growth was observed when 500 µM ancymidol-treated cultures were supplemented with 100 µM GA3. Ancymidol impaired the accumulation of cellulose in cell walls, as monitored by FTIR spectroscopy. Cells treated with 500 µM ancymidol showed a ~ 60% reduction in cellulose content, with no further change as the ancymidol concentration increased. Cellulose content was partially restored by 100 µM GA3. Radiolabeling experiments confirmed that ancymidol reduced the incorporation of [14C]glucose into α-cellulose and this reduction was not reverted by the simultaneous application of GA3. RT-PCR analysis indicated that the cellulose biosynthesis inhibition caused by ancymidol is not related to a downregulation of ZmCesA gene expression. Additionally, ancymidol treatment increased the incorporation of [3H]arabinose into a hemicellulose-enriched fraction, and up-regulated ZmIRX9 and ZmIRX10L gene expression, indicating an enhancement in the biosynthesis of arabinoxylans as a compensatory response to cellulose reduction.

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Abbreviations

ANW:

Acetic acid–nitric acid–water

CBI:

Cellulose biosynthesis inhibitor

CDTA:

Cyclohexane-trans-1,2-diamine-N,N,N′,N′-tetraacetic acid sodium salt

CesA :

Cellulose synthase gene

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Acknowledgements

The authors thank Dr. Ana Alonso-Simón for her helpful scientific discussion, and Denise Phelps for the English revision of the manuscript. This study was supported by Grants from the Spanish Ministry of Science and Innovation (CGL2008-02470 and AGL2011-30545-C02-02). RM and AL received funding through Ph.D. Grants from the Spanish Ministry of Science and Innovation FPU program, and the University of León, respectively.

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Authors and Affiliations

  1. Departamento de Ingeniería y Ciencias Agrarias, Área de Fisiología Vegetal, Universidad de León, 24071, León, Spain

    J. Mabel Hernández-Altamirano, Asier Largo-Gosens, Romina Martínez-Rubio, Diego Pereda, Jesús M. Álvarez, José L. Acebes, Antonio Encina & Penélope García-Angulo

  2. Centro de Biotecnología Vegetal, Facultad de Ciencias Biológicas, Universidad Nacional Andrés Bello, 8370146, Santiago, Chile

    Asier Largo-Gosens

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  1. J. Mabel Hernández-Altamirano
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  2. Asier Largo-Gosens
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  3. Romina Martínez-Rubio
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  4. Diego Pereda
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  5. Jesús M. Álvarez
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  6. José L. Acebes
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  7. Antonio Encina
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  8. Penélope García-Angulo
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Correspondence to José L. Acebes.

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Hernández-Altamirano, J.M., Largo-Gosens, A., Martínez-Rubio, R. et al. Effect of ancymidol on cell wall metabolism in growing maize cells. Planta 247, 987–999 (2018). https://doi.org/10.1007/s00425-018-2840-y

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