Revealing the molecular mechanisms of zinc accumulation and zinc deficiency responses in quinoa, analyzed by high-throughput gene expression profiling under zinc depletion and resupply

Abstract

Zinc (Zn) is an essential micronutrient for plant growth and development, but the soil available Zn is low in arable land worldwide. Therefore, crop Zn deficiency is a serious issue that threatens the sustainable development of agriculture. Quinoa (Chenopodium quinoa Willd.) is a high-efficiency Zn utilization crop. However, the molecular regulatory mechanisms underlying Zn uptake and Zn deficiency response in quinoa remain largely unclear. Here, using the method of Zn depletion and resupply, we investigated Zn deficiency responses in the hydroponic-grown quinoa seedlings by integrating physiol-biochemical and transcriptomic analyses. Zn depletion leads to H2O2 accumulation and lipid peroxidation in plants. Accordingly, the increased enzyme activities of superoxide dismutase and peroxidase alleviate Zn deficiency-induced oxidative damage in quinoa roots. Subsequently, a genome-wide transcriptome analysis revealed that the expression of genes encoding Zn sensors bZIP19/23 and metal transporters was upregulated in Zn-depleted plants but downregulated in Zn-resupplied plants. Interestingly, the high expression of several iron (Fe) deficiency-responsive transcription factors/transcription regulator genes may not be induced by Fe status in Zn-depleted plants, suggesting that the expression of these genes may be directly induced by Zn deficiency and subsequently regulate micronutrient homeostasis in plants. Zn depletion decreased the contents of indoacetic acid, trans-zeatin-riboside, abscisic acid and salicylic acid 2-O-β-d-glucose but increased the jasmonic acid content in quinoa roots. These results collectively indicated that Zn deficiency affects plant growth and development by modulating phytohormone pathways. Our results provide comprehensive insight into the mechanism of Zn uptake and Zn deficiency response in quinoa and provide a theoretical basis for breeding Zn-efficient crops.