Abstract

BackgroundRice (Oryza sativa L.) is highly susceptible to iron (Fe) deficiency due to low secretion levels of the mugineic acid (MA) family phytosiderophore (PS) 2′-deoxymugineic acid (DMA) into the rhizosphere. The low levels of DMA secreted by rice have proved challenging to measure and, therefore, the pattern of DMA secretion under Fe deficiency has been less extensively studied relative to other graminaceous monocot species that secrete high levels of PS, such as barley (Hordeum vulgare L.).ResultsGene expression and metabolite analyses were used to characterise diurnal changes occurring during the Fe deficiency response of rice. Iron deficiency inducible genes involved in root DMA biosynthesis and secretion followed a diurnal pattern with peak induction occurring 3–5 h after the onset of light; a result consistent with that of other Strategy II plant species such as barley and wheat. Furthermore, triple quadrupole mass spectrometry identified 3–5 h after the onset of light as peak time of DMA secretion from Fe-deficient rice roots. Metabolite profiling identified accumulation of amines associated with metal chelation, metal translocation and plant oxidative stress responses occurring with peak induction 10–12 h after the onset of light.ConclusionThe results of this study confirmed that rice shares a similar peak time of Fe deficiency associated induction of DMA secretion compared to other Strategy II plant species but has less prominent daily fluctuations of DMA secretion. It also revealed metabolic changes associated with the remediation of Fe deficiency and mitigation of damage from resulting stress in rice roots. This study complements previous studies on the genetic changes in response to Fe deficiency in rice and constitutes an important advance towards our understanding of the molecular mechanisms underlying the rice Fe deficiency response.

Highlights

  • Rice (Oryza sativa L.) is highly susceptible to iron (Fe) deficiency due to low secretion levels of the mugineic acid (MA) family phytosiderophore (PS) 2′-deoxymugineic acid (DMA) into the rhizosphere

  • Expression of Genes Involved in the Strategy II Response in Fe-deficient Rice Roots Analysis of root transcripts (Additional file 1: Table S1A) by quantitative real time PCR identified that Fe deficiency resulted in a significant increase in the expression of OsNAS1 (p ≤ 0.001), OsNAS2 (p ≤ 0.001), OsNAS3 (p ≤ 0.001), OsNAAT1 (p ≤ 0.001), OsDMAS1 (p ≤ 0.001), and OsYSL15 (p = 0.006), but no significant change in the expression of OsTOM1 (p = 0.054)

  • Fe deficiency promoted increased expression of genes involved in nicotianamine (NA) and DMA biosynthesis, DMA secretion, and uptake of Fe3+-DMA complexes following a diurnal pattern with a peak time of induction 3–5 h after the onset of light

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Summary

Introduction

Rice (Oryza sativa L.) is highly susceptible to iron (Fe) deficiency due to low secretion levels of the mugineic acid (MA) family phytosiderophore (PS) 2′-deoxymugineic acid (DMA) into the rhizosphere. Iron is the functional cofactor for the heme containing hemoprotein superfamily of enzymes involved in photosynthesis, respiration, DNA synthesis (Michel and Pistorius 2004) and antioxidants including peroxidases (Zaharieva and Abadía 2003). Antioxidants quench reactive oxygen species (ROS) which are produced as an inevitable consequence of photosynthesis (Parida and Das 2005) and to a lesser extent due to respiration (Gill and Tuteja 2010). Cellular stress induced by Fe deficiency results in impaired antioxidant activity due to absence of the required catalytic Fe, leading to an increased abundance of cellular ROS (Becana et al 1998; Iturbe-Ormaetxe et al 1995). Fe homeostasis must be tightly regulated in plants to prevent Fe-deficiency-induced oxidative damage to proteins and lipids (Sun et al 2007)

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