Local endoreduplication of the host is a conserved process during Phytomyxea-host interaction

Abstract

Endoreduplication is a modified cell cycle in which cells duplicate their DNA without subsequent mitosis. This process is common in plants and can also be found in other organisms like algae and animals. Biotrophic plant pathogens have been shown to induce endoreduplication in their host to gain space and/or nutrients. Phytomyxea (divided into the Plasmodiophorida, the Phagomyxida, and the Marinomyxa clade) are obligate biotrophic parasites of plants, diatoms, brown algae, and oomycetes. Here, we tested if phytomyxids induce local endoreduplication in two distant hosts (plants and brown algae). By combining fluorescent in situ hybridisation (FISH) coupled with nuclear area measurements and flow cytometry, we confirmed that endoreduplication is induced by Plasmodiophora brassicae (Plasmodiophorida) in infected plants and demonstrate this process in combination with Maullinia ectocarpii and Maullinia braseltonii (Phagomyxida) in brown algae. We identified molecular signatures of endoreduplication in RNA-seq datasets of P. brassicae-infected Brassica oleraceae and M. ectocarpii-infected Ectocarpus siliculosus. Cell cycle switch proteins (CCS52A1 and B in plants and CCS52 in algae) as well as the protein kinase WEE1 (in plants) were identified as genes potentially important for the phytomyxean-induced switch from the mitotic cell cycle to the endocycle. Their expression pattern changed in infected plants and brown algae accordingly. In this study we expand the knowledge on Phytomyxea-host interactions by showing that induced endoreduplication in the host is a conserved feature in phytomyxid infections. The induction of this cellular mechanism by phytomyxid parasites in phylogenetically distant hosts further points at a fundamental importance of endoreduplication in these biotrophic interactions.