An rbcL mRNA-binding protein is associated with C(3) to C(4) evolution and light-induced production of Rubisco in Flaveria

Nuclear-encoded RLSB protein binds chloroplastic rbcL mRNA encoding the Rubisco large subunit. RLSB is highly conserved across all groups of land plants and is associated with positive post-transcriptional regulation of rbcL expression. In C(3) leaves, RLSB and Rubisco occur in all chlorenchyma cell chloroplasts, while in C(4) leaves these accumulate only within bundle sheath (BS) chloroplasts. RLSB’s role in rbcL expression makes modification of its localization a likely prerequisite for the evolutionary restriction of Rubisco to BS cells. Taking advantage of evolutionarily conserved RLSB orthologs in several C(3), C(3)–C(4), C(4)-like, and C(4) photosynthetic types within the genus Flaveria, we show that low level RLSB sequence divergence and modification to BS specificity coincided with ontogeny of Rubisco specificity and Kranz anatomy during C(3) to C(4) evolution. In both C(3) and C(4) species, Rubisco production reflected RLSB production in all cell types, tissues, and conditions examined. Co-localization occurred only in photosynthetic tissues, and both proteins were co-ordinately induced by light at post-transcriptional levels. RLSB is currently the only mRNA-binding protein to be associated with rbcL gene regulation in any plant, with variations in sequence and acquisition of cell type specificity reflecting the progression of C(4) evolution within the genus Flaveria.