Abstract

The transition zone (TZ) of the root apex is the perception site of Al toxicity. Here, we show that exposure of Arabidopsis thaliana roots to Al induces a localized enhancement of auxin signaling in the root-apex TZ that is dependent on TAA1, which encodes a Trp aminotransferase and regulates auxin biosynthesis. TAA1 is specifically upregulated in the root-apex TZ in response to Al treatment, thus mediating local auxin biosynthesis and inhibition of root growth. The TAA1-regulated local auxin biosynthesis in the root-apex TZ in response to Al stress is dependent on ethylene, as revealed by manipulating ethylene homeostasis via the precursor of ethylene biosynthesis 1-aminocyclopropane-1-carboxylic acid, the inhibitor of ethylene biosynthesis aminoethoxyvinylglycine, or mutant analysis. In response to Al stress, ethylene signaling locally upregulates TAA1 expression and thus auxin responses in the TZ and results in auxin-regulated root growth inhibition through a number of auxin response factors (ARFs). In particular, ARF10 and ARF16 are important in the regulation of cell wall modification-related genes. Our study suggests a mechanism underlying how environmental cues affect root growth plasticity through influencing local auxin biosynthesis and signaling.

Highlights

  • Al is the most abundant metal in the earth’s crust

  • Further time-course analysis of DR5rev:green fluorescent protein (GFP) signals in the presence of 6 mM Al revealed that the DR5rev:GFP signals in the transition zone (TZ) increased until 12 h and, thereafter, remarkably decreased and even disappeared after 7 d of exposure to toxic Al (Supplemental Figure 2), suggesting that auxin may act as an early Al-responsive signal to regulate the Al-induced root growth inhibition

  • To test whether the Al-induced auxin reporter DR5rev:GFP signaling maximum in the TZ reflects the endogenous increased auxin level, we measured the concentration of indole-3-acetic acid (IAA) in 1-mm-long root tips

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Summary

Introduction

Al is the most abundant metal in the earth’s crust. In acidic soils (pH < 5), the phytotoxic Al3+ ion becomes increasingly soluble and becomes a significant constraint on crop productivity. The root apex is the major target site of Al toxicity (Ryan and Kochian, 1993); in maize (Zea mays), the distal part of the root-apex transition zone (TZ), located between the apical meristem and the basal elongation region, is the most Al-sensitive part of the root (Sivaguru and Horst, 1998), and a similar zone is involved in both common bean (Phaseolus vulgaris) (Rangel et al, 2007) and Arabidopsis thaliana (Illés et al, 2006). The importance of the distal part of the root TZ in the response to Al toxicity has been confirmed in sorghum (Sorghum bicolor) by the demonstration that it is the site of reactive oxygen species production (Sivaguru et al, 2013)

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