Difference in Nitrogen Starvation-Inducible Expression Patterns among Phylogenetically Diverse Ammonium Transporter Genes in the Red Seaweed Pyropia yezoensis

Abstract

Nitrogen deficiency induces senescence and the expression of genes encoding ammonium transporters (AMTs) in terrestrial plants where the AMT family is subdivided into AMT1 and AMT2 subfamilies. Nitrogen starvation in the red seaweed Pyropia yezoensis causes senescence-like discoloration. In this study, we identified five genes in P. yezoensis encoding AMT domain-containing proteins, which were phylogenetically categorized into the AMT1 subfamily. We also found a gene encoding a Rhesus protein (Rh) that was related to, but diverged from, AMTs. Moreover, our phylogenetic analysis showed that AMT domain-containing proteins from micro- and macro-algae belonged to either the AMT1 or Rh subfamily, indicating the absence of AMT2 in algae. Gene expression analyses revealed the presence of gametophyte- and sporophyte-specific AMT1 genes that were up-regulated transiently and continually, respectively, under nitrogen-deficient conditions. In addition, up-regulated sporophyte-specific gene expression was suppressed when nitrogen was resupplied. Accordingly, an expansion of the ancient AMT gene has produced AMT1 functional variants differing in temporal and nitrogen starvation-in- ducible expression patterns during the life cycle of P. yezoensis. These findings help elucidate the unique nutrition starvation responses involving functionally diverse AMT1 and Rh subfamilies in red seaweed.