Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen

Understanding how plants balance between enabling microbial symbionts and fending off pathogens has direct implications both for basic plant biology and optimal use of crop plants in agriculture. The degree to which the processes associated with these two types of interactions overlap is poorly known. Recent studies revealed that symbiotic and pathogenic filamentous microbes require common plant genetic elements to establish colonization (Wang et al., 2012; Rey et al., 2013), supporting the long-held view that plants have evolved the ability to accommodate microbes (Parniske, 2000) and that pathogens have exploited these pathways. However, the extent to which plant genes implicated in fungal or bacterial symbioses are involved in interactions with biotrophic pathogens is unknown and research has been hampered by the lack of suitable common host experimental systems.

Phytophthora palmivora, a root-infecting oomycete, is an aggressive biotrophic pathogen of Medicago truncatula, a model legume plant that is widely used in symbiosis research. Expression of fluorescent proteins in P. palmivora permits visualization of infection structures in M. truncatula roots. During its initial biotrophic colonization of M. truncatula roots which lasts until c. 48 h post-inoculation (hpi), P. palmivora zoospores expressing tdtomato red fluorescent protein (isolate AJ-td) germinate and form appressoria to penetrate the epidermis followed by rapid colonization of the root cortex apoplast and projection of short specialized hyphae, termed haustoria into plant cells (Fig. 1a). P. palmivora infection is accompanied by visible disease development in M. truncatula seedlings consisting of translucent tissue at the root tip at 2 d post-inoculation (dpi) and tissue browning in upper parts of the root at 3 dpi. (Fig. 1b, see also Supporting Information Methods S1). Concomitant with a switch to a nectrophic lifestyle, the pathogen enters the vasculature (Fig. 1a).