Mechanisms of growth and patterns of gene expression in oxygen-deprived rice coleoptiles

Reena Narsai, Joshua M. Edwards, Thomas H. Roberts, James Whelan, Gregory H. Joss, Brian J. Atwell*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

28 Citations (Scopus)

Abstract

Coleoptiles of rice (Oryza sativa) seedlings grown under water commonly elongate by up to 1 mm h-1 to reach the atmosphere. We initially analysed this highly specialized phenomenon by measuring epidermal cell lengths along the coleoptile axis to determine elongation rates. This revealed a cohort of cells in the basal zone that elongated rapidly following emergence from the embryo, reaching 200 μm within 12 h. After filming coleoptiles in vivo for a day, kinematic analysis was applied. Eight time-sliced 'segments' were defined by their emergence from the embryo at four-hourly intervals, revealing a mathematically simple growth model. Each segment entering the coleoptile from the embryo elongated at a constant velocity, resulting in accelerating growth for the entire organ. Consistent with the epidermal cell lengths, relative rates of elongation (mm mm-1 h-1) were tenfold greater in the small, newly emerged basal segments than the older distal tip segments. This steep axial gradient defined two contrasting growth zones (bases versus tips) in which we measured ATP production and protein, RNA and DNA content, and analysed the global transcriptome under steady-state normoxia, hypoxia (3% O2) and anoxia. Determination of the transcriptome revealed tip-specific induction of genes encoding TCP [Teosinte Branched1 (Tb1) of maize, Cycloidea (Cyc), and Proliferating Cell Factor (Pcf)] transcription factors, RNA helicases, ribosomal proteins and proteins involved in protein folding, whilst expression of F-box domain-containing proteins in the ubiquitin E3-SCF complex (Skp, Cullin, F-box containing complex) was induced specifically in bases under low oxygen conditions. We ascribed the sustained elongation under hypoxia to hypoxia-specific responses such as controlled suppression of photosystem components and induction of RNA binding/splicing functions, indicating preferential allocation of energy to cell extension. Significance Statement We present a global gene expression study linked with biophysics. It reveals a comprehensive description of how submerged rice coleoptiles elongate in the days after germination. The approaches include epidermal cell length analysis (providing local growth rates) with kinematics (video analysis). By applying steady-state oxygen treatments that include anoxia and hypoxia, we then contrast gene expression patterns in contrasting fast- and slow-growing zones to explain how coleoptiles elongate when submerged.

Original languageEnglish
Pages (from-to)25-40
Number of pages16
JournalPlant Journal
Volume82
Issue number1
DOIs
Publication statusPublished - 1 Apr 2015

Keywords

  • anoxia
  • coleoptile
  • elongation
  • hypoxia
  • Oryza sativa
  • rice
  • submergence

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