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

Abstract

These authors contributed equally to this work. SUMMARYColeoptiles of rice (Oryza sativa) seedlings grown under water commonly elongate by up to 1 mm h À1 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 lm 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 À1 h À1 ) 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% O 2 ) 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.

RNA-Seq Analysis of Diverse Rice Genotypes to Identify the Genes Controlling Coleoptile Growth during Submerged Germination

“…These experiments were performed at various O 2 levels, and used expression microarrays to detect the transcription profiles of single rice varieties. The results of these studies revealed that a number of common molecular mechanisms are involved in coleoptile growth, including carbohydrate metabolism, fermentation, hormone induction, cell division, and expansion (Lasanthi-Kudahettige et al, 2007; Huang et al, 2009; Shingaki-Wells et al, 2011; Narsai et al, 2015). Another recent study analyzed gene expression in the tips and basal segments of O 2 -deprived rice coleoptiles, identified the presence of region-specific gene induction, and provided a detailed picture of differential metabolic activities along the length of the coleoptile under normoxic (air), hypoxic (3% O 2 ), and anoxic conditions (Narsai et al, 2015).…”

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

“…Fundamental knowledge of the genetic, physiological, and molecular regulation of these traits is not only of general interest but essential to improve the tolerance of many economically relevant crops, most of which are very sensitive to floods (Voesenek et al, 2014). The genetic and molecular regulation of flood-adaptive strategies has been studied most extensively in semiaquatic flood-tolerant species of the genera Oryza, Rorippa, and Rumex Hattori et al, 2009;Lee et al, 2009;Sasidharan et al, 2013;van Veen et al, 2013van Veen et al, , 2014aNarsai et al, 2015).…”

Alternative splicing and translation play important roles in parallel with transcriptional regulation during rice hypoxic germination

“…Transcriptomic studies have shown that low oxygen induces a myriad of gene responsiveness in terms of transcript abundance (Lasanthi-Kudahettige et al, 2007; Narsai et al, 2009; Narsai et al, 2011; Sadiq et al, 2011; Narsai et al, 2015; Hsu and Tung, 2017). Accordingly, transcriptional regulation in oxygen sensing pathways has been extensively studied in plants.…”

“…With the development of large profiling techniques, considerable efforts have been made to study the global transcripts changes, protein abundance and metabolic variation during rice hypoxic germination (Lasanthi-Kudahettige et al, 2007; Narsai et al, 2009; Narsai et al, 2011; Sadiq et al, 2011; Narsai et al, 2015; Hsu and Tung, 2017). Although comparative analysis indicates that part of the hypoxic responsive pathways are conserved among several species (Narsai et al, 2011), the mechanism of adult flooding tolerance may be largely different from that of seed flooding tolerance (Lu et al, 2007; Lee et al, 2009).…”