Original Article

Planta

, Volume 223, Issue 6, pp 1315-1328

First online:

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

  • Shizue MatsubaraAffiliated withInstitut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich Email author 
  • , Vaughan HurryAffiliated withUmeå Plant Science Centre, Department of Plant Physiology, Umeå University
  • , Nathalie DruartAffiliated withUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
  • , Catherine BenedictAffiliated withUmeå Plant Science Centre, Department of Plant Physiology, Umeå University
  • , Ingar JanzikAffiliated withInstitut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich
  • , Andrés Chavarría-KrauserAffiliated withInstitut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich
  • , Achim WalterAffiliated withInstitut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich
  • , Ulrich SchurrAffiliated withInstitut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich

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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.

Keywords

Cell cycle Cytoplasmic growth Leaf growth Microarray Populus Ribosomal protein