A two-component signature determines which rust fungi secreted proteins are translocated into the cells of the host plant

Abstract

Rust diseases of plants are caused by parasitic fungi that feed off living plant cells by means of haustoria that form within plant cells. These haustoria also secrete a large number of proteins, some of which remain in the matrix surrounding the haustoria while others are translocated through a membrane into the cytoplasm of the plant cell. These latter proteins would be expected to possess a signature marking them out for translocation but, to date, no such signature has been identified. An examination of a set of wheat rust proteins known to be translocated to the cytoplasm of the wheat cell, together with an analysis of 1208 wheat stem rust (Puccinia graminis f. sp. tritici) secretome proteins, provides evidence that the translocation signature contains two components. The first component consists of a positively-charged amino acid at position 1, 2 or 3 (and possibly 4 or greater) upstream of the hydrophobic region in the signal peptide. The second component consists of a positively-charged amino acid at position 21 downstream of the signal peptide. A similar analysis of flax rust (Melampsora lini) secretome proteins indicates that the first component is the same as that of the wheat stem rust secretome proteins but that the second component consists of a positively-charged amino acid at position (16)17-20 downstream of the signal peptide. The flax rust signature may also be employed by wheat stem rust in its pycnial stage when growing on its alternate dicot host, barberry. Being able to identify which rust haustorial secreted proteins go to the plant cytoplasm and which to the extrahaustorial matrix should facilitate work aimed at identifying the function of each of the secreted proteins and, also, work aimed at elucidating the translocation mechanism, an understanding of which could open up new approaches to rust control.