C(3) cotyledons are followed by C(4) leaves: intra-individual transcriptome analysis of Salsola soda (Chenopodiaceae)

Some species of Salsoleae (Chenopodiaceae) convert from C(3) photosynthesis during the seedling stage to the C(4) pathway in adult leaves. This unique developmental transition of photosynthetic pathways offers the exceptional opportunity to follow the development of the derived C(4) syndrome from the C(3) condition within individual plants, avoiding phylogenetic noise. Here we investigate Salsola soda, a little-studied species from tribe Salsoleae, using an ontogenetic approach. Anatomical sections, carbon isotope (δ(13)C) values, transcriptome analysis by means of mRNA sequencing, and protein levels of the key C(4) enzyme phosphoenolpyruvate carboxylase (PEPC) were examined from seed to adult plant stages. Despite a previous report, our results based on δ(13)C values, anatomy and transcriptomics clearly indicate a C(3) phase during the cotyledon stage. During this stage, the entire transcriptional repertoire of the C(4) NADP-malic enzyme type is detected at low levels compared to a significant increase in true leaves. In contrast, abundance of transcripts encoding most of the major photorespiratory enzymes is not significantly decreased in leaves compared to cotyledons. PEPC polypeptide was detected only in leaves, correlating with increased PEPC transcript abundance from the cotyledon to leaf stage.