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The  xantha  marker trait, which is controlled by a down-regulating epi-mutation of  OsGUN4 , has been applied to the production of hybrid rice. However, the molecular basis for the ability of  xantha  mutants to attain high photosynthetic capacity even with decreased chlorophyll contents has not been characterized. In the present study, we observed that the total chlorophyll content of the  xantha  mutant was only 27.2% of that of the wild-type (WT) plants. However, the  xantha  mutant still accumulated 59.9% of the WT δ-aminolevulinic acid content, 72.8% of the WT Mg-protoporphyrin IX content, and 63.0% of the WT protochlorophyllide  a  content. Additionally, the protoporphyrin IX and heme contents in the mutant increased to 155.0 and 160.0%, respectively, of the WT levels. A search for homologs resulted in the identification of 124 rice genes involved in tetrapyrrole biosynthesis and photosynthesis. With the exception of  OsGUN4 ,  OsHO-1 , and  OsHO-2 , the expression levels of the genes involved in tetrapyrrole biosynthesis were significantly higher in the  xantha  mutant than in the WT plants, as were all 72 photosynthesis-associated nuclear genes. In contrast, there were no differences between the  xantha  mutant and WT plants regarding the expression of all 22 photosynthesis-associated chloroplast genes. Furthermore, the abundance of  1 O 2  and the expression levels of  1 O 2 -related genes were lower in the  xantha  mutant than in the WT plants, indicating  1 O 2 -mediated retrograde signaling was repressed in the mutant plants. These results suggested that the abundance of protoporphyrin IX used for chlorophyll synthesis decreased in the mutant, which ultimately decreased the amount of chlorophyll in the  xantha  mutant. Additionally, the up-regulated expression of photosynthesis-associated nuclear genes enabled the mutant to attain a high photosynthetic capacity. Our findings confirm that OsGUN4 plays an important role in tetrapyrrole biosynthesis and photosynthesis in rice. GUN4, chlorophyll synthesis pathways, and photosynthetic activities are highly conserved in plants and hence, novel traits (e.g.,  xantha  marker trait) may be generated in other cereal crops by modifying the  GUN4  gene.

The xantha Marker Trait Is Associated with Altered Tetrapyrrole Biosynthesis and Deregulated Transcription of PhANGs in Rice