Nickel Toxicity Targets Cell Wall-Related Processes and PIN2-MeaiaLed Auxin Transport to Inhibit Root Elongation and Gravitropic Responses in Arabidopsis

Contamin; 'ion of soils with heavy metals, such as nickel (Ni), is a major environmental concern due to increasing pollution from industrial activities, burning of fossil fuels, incorrect disposal of sewage sludge, excessive manure application and the use of fertilizers and pesticides in agriculture. Excess Ni induces leaf chlorosis and inhibits plant growth, but the mechanisms underlying growth inhibition remain largely unknown. A detailed analysis of root development in Arabidopsis thaliana in the presence of Ni revealed that this heavy metal induces gravitropic defects and locally inhibits root growth by suppressing cell elongation without significantly disrupting the integrity of the stem cell niche. The analysis of auxin-responsive reporters revealed that excess Ni inhibits shootward auxin distribution. Furthermore, we found that PIN2 is very sensitive to Ni, as the presence of this heavy metal rapidly reduced PIN2 levels in roots. A transcriptome analysis also showed that Ni affects the expression of many genes associated with plant cell walls and that Ni-induced transcriptional changes are largely independent of iron (Fe). In addition, we raised evidence that excess Ni increases the accumulation of reactive oxygen species and disturbs the integrity and orientation of microtubules. Together, our results highlight which processes are primarily targeted by Ni to alter root growth and development.