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Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth

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Abstract

Growing leaves do not expand at a constant rate but exhibit pronounced diel growth rhythms. However, the mechanisms giving rise to distinct diel growth dynamics in different species are still largely unknown. As a first step towards identifying genes controlling rate and timing of leaf growth, we analysed the transcriptomes of rapidly expanding and fully expanded leaves of Populus deltoides Bartr. ex. Marsh at points of high and low expansion at night. Tissues with well defined temporal growth rates were harvested using an online growth-monitoring system based on a digital image sequence processing method developed for quantitative mapping of dicot leaf growth. Unlike plants studied previously, leaf growth in P. deltoides was characterised by lack of a base-tip gradient across the lamina, and by maximal and minimal growth at dusk and dawn, respectively. Microarray analysis revealed that the nocturnal decline in growth coincided with a concerted down-regulation of ribosomal protein genes, indicating deceleration of cytoplasmic growth. In a subsequent time-course experiment, Northern blotting and real-time RT-PCR confirmed that the ribosomal protein gene RPL12 and a cell-cycle gene H2B were down-regulated after midnight following a decrease in cellular carbohydrate concentrations. Thus, we propose that the spatio-temporal growth pattern in leaves of P. deltoides primarily arises from cytoplasmic growth whose activity increases from afternoon to midnight and thereafter decreases in this species.

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Abbreviations

LPI:

Leaf plastochron index

M:

Mature leaves

RGR:

Relative growth rate

RP:

Ribosomal protein

Y:

Young leaves

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Acknowledgements

Kind assistance by Ingela Sandström, Andreas Sjödin (UPSC, Umeå) and Volker Wendisch (FZJ, Jülich) for the microarray analysis, Katharina Klug and Kate Morrissey (FZJ, Jülich) for RNA analyses, and Maja Christ and Kerstin Nagel (FZJ, Jülich) for carbohydrate assay is greatly acknowledged. The microarray experiment at UPSC was supported by Forest Research Environment (FORE, Umeå), the European Community’s programme “Improving the Human Research Potential and the Socio-Economic Knowledge Base”, the “Project-based Personnel Exchange Programme” of Deutscher Akademischer Austauschdienst (DAAD), and by a grant from the Swedish Forestry and Agricultural Research Council to VH.

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Authors and Affiliations

  1. Institut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich, 52425, Jülich, Germany

    Shizue Matsubara, Ingar Janzik, Andrés Chavarría-Krauser, Achim Walter & Ulrich Schurr

  2. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187, Umeå, Sweden

    Vaughan Hurry & Catherine Benedict

  3. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden

    Nathalie Druart

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  1. Shizue Matsubara
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Correspondence to Shizue Matsubara.

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Matsubara, S., Hurry, V., Druart, N. et al. Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth. Planta 223, 1315–1328 (2006). https://doi.org/10.1007/s00425-005-0181-0

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