Abstract
Auxin is necessary for the inhibition of root growth induced by aluminium (Al) stress, however the molecular mechanism controlling this is largely unknown. Here, we report that YUCCA (YUC), which encodes flavin monooxygenase-like proteins, regulates local auxin biosynthesis in the root apex transition zone (TZ) in response to Al stress. Al stress up-regulates YUC3/5/7/8/9 in the root-apex TZ, which we show results in the accumulation of auxin in the root-apex TZ and root-growth inhibition during the Al stress response. These Al-dependent changes in the regulation of YUCs in the root-apex TZ and YUC-regulated root growth inhibition are dependent on ethylene signalling. Increasing or disruption of ethylene signalling caused either enhanced or reduced up-regulation, respectively, of YUCs in root-apex TZ in response to Al stress. In addition, ethylene enhanced root growth inhibition under Al stress was strongly alleviated in yuc mutants or by co-treatment with yucasin, an inhibitor of YUC activity, suggesting a downstream role of YUCs in this process. Moreover, ethylene-insensitive 3 (EIN3) is involved into the direct regulation of YUC9 transcription in this process. Furthermore, we demonstrated that PHYTOCHROME INTERACTING FACTOR4 (PIF4) functions as a transcriptional activator for YUC5/8/9. PIF4 promotes Al-inhibited primary root growth by regulating the local expression of YUCs and auxin signal in the root-apex TZ. The Al–induced expression of PIF4 in root TZ acts downstream of ethylene signalling. Taken together, our results highlight a regulatory cascade for YUCs-regulated local auxin biosynthesis in the root-apex TZ mediating root growth inhibition in response to Al stress.
Highlights
Aluminium is highly abundant in the soil, but only presents toxicity problems to plants in acid soils, where it becomes solubilized into the Al3+ ion
The phytohormone auxin, which is synthesized mainly through TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and YUCCA (YUC) flavin monooxygenase-like proteins, has an important role in the inhibition of root growth induced by aluminium (Al) stress
TAA1 was recently shown to be locally induced in the root-apex transition-zone involves in aluminium-induced Arabidopsis root growth inhibition
Summary
Aluminium is highly abundant in the soil, but only presents toxicity problems to plants in acid (pH 5) soils, where it becomes solubilized into the Al3+ ion. Modest levels of Al3+ in the soil are sufficient to inhibit root growth in most species [1,2,3,4]. A variety of plant growth and developmental processes are mediated by the phytohormone auxin, which is present for the most part as indole-3-acetic acid (IAA). The YUCCA (YUC) family of flavin-containing mono-oxygenases and the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) family of aminotransferases are both key enzymes in this pathway [15,16,17,18,19]. TAA enzymes catalyse the conversion of tryptophan to indole-3-pyruvate (IPyA), while YUCs are involved in the conversion of IPyA to IAA, a rate-limiting step in the IPyA pathway [18,19,20,21,22]
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