Mosaic symptoms are commonly observed in virus-infected plants. However, the underlying mechanism by which viruses cause mosaic symptoms as well as the key regulator(s) involved in this process remain unclear. Here, we investigate maize dwarf mosaic disease caused by sugarcane mosaic virus (SCMV). We find that the manifestation of mosaic symptoms in SCMV-infected maize plants requires light illumination and is correlated with mitochondrial reactive oxidative species (mROS) accumulation. The transcriptomic and metabolomic analyses results together with the genetic and cytopathological evidence indicate that malate and malate circulation pathways play essential roles in promoting mosaic symptom development. Specifically, at the pre-symptomatic infection stage or infection front, SCMV infection elevates the enzymatic activity of pyruvate orthophosphate dikinase by decreasing the phosphorylation of threonine527 under light, resulting in malate overproduction and subsequent mROS accumulation. Our findings indicate that activated malate circulation contributes to the manifestation of light-dependent mosaic symptoms via mROS.

Histone modifications play important roles in regulating the expression of C4 photosynthetic genes. Given that all enzymes required for the C4 photosynthesis pathway are present in C3 plants, it has been hypothesized that this expression regulatory mechanism has been conserved. However, the relationship between histone modification and the expression of homologs of C4 photosynthetic enzyme genes has not been well determined in C3 plants. In the present study, we cloned nine hybrid poplar (Populus simonii × Populus nigra) homologs of maize (Zea mays) C4 photosynthetic enzyme genes, carbonic anhydrase (CA), pyruvate orthophosphate dikinase (PPDK), phosphoenolpyruvate carboxykinase (PCK), and phosphoenolpyruvate carboxylase (PEPC), and investigated the correlation between the expression levels of these genes and the levels of promoter histone acetylation modifications in four vegetative tissues. We found that poplar homologs of C4 homologous genes had tissue-dependent expression patterns that were mostly well-correlated with the level of histone acetylation modification (H3K9ac and H4K5ac) determined by chromatin immunoprecipitation assays. Treatment with the histone deacetylase inhibitor trichostatin A further confirmed the role of histone acetylation in the regulation of the nine target genes. Collectively, these results suggest that both H3K9ac and H4K5ac positively regulate the tissue-dependent expression pattern of the PsnCAs, PsnPPDKs, PsnPCKs, and PsnPEPCs genes and that this regulatory mechanism seems to be conserved among the C3 and C4 species. Our findings provide new insight that will aid efforts to modify the expression pattern of these homologs of C4 genes to engineer C4 plants from C3 plants.