Massive Loss of DNA Methylation in Nitrogen-, but Not in Phosphorus-Deficient Zea mays Roots Is Poorly Correlated With Gene Expression Differences

DNA methylation in plants plays a role in transposon silencing, genome stability and gene expression regulation. Environmental factors alter the methylation pattern of DNA and recently nutrient stresses, such as phosphate starvation, were shown to alter DNA methylation. Furthermore, DNA methylation had been frequently addressed in plants with notably small genomes that are poor in transposons. Here, we compare part of the DNA methylome of nitrogen- and phosphorus-deficient maize roots by reduced representation sequencing and analyze their relationship with gene expression under prolonged stresses. Tremendous DNA methylation loss was encountered in maize under nitrogen-deficiency, but much less with phosphorus-deficiency. This occurred only in the symmetrical cytosine context, predominantly in CG context, but also in the CHG context. In contrast to other plants, differential methylation in the more flexible CHH context was essentially absent. In both deficiency conditions a similar number of differentially expressed genes were found and differentially methylated regions (DMRs) were predominantly identified in transposable elements (TEs). A minor fraction of such DMRs was associated with altered gene expression of nearby genes. Interestingly, although these TEs were mostly hypomethylated, they were associated with both up- or down regulated gene expression. Our results suggest a different methylome regulation in maize compared to rice and Arabidopsis upon nutrient deficiencies and point to highly nutrient- and species-specific dynamics of genomic DNA methylation. Description of Significance: DNA methylation suppresses transposons in plant genomes, but was also associated with other genome protective functions and gene expression regulation. Recently it was shown that DNA methylation dynamically responds to several abiotic and biotic environmental factors, but to a large instance, DNA methylation is also heritable. DNA methylation changes have also been reported under phosphorus starvation in rice and Arabidopsis, but its relation with other nutrients and its importance for individual gene expression remains unclear. Here, DNA methylation changes upon the deficiency of two major essential nutrients, nitrogen and phosphorus, were studied in parallel with gene expression responses in maize roots. We show context, nutrient- and species-specific patterns in the methylome, as well as its relation with the nutrient-deficiency transcriptome. While cases of differentially methylated regions in the vicinity of differentially expressed genes were apparent, both positive and negative roles on the gene expression were identified, irrespective of the context.