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Developmental reprogramming by parasitic nematodes

The plant root interface is constantly subject to a dynamic range of interactions with other organisms. These can be beneficial in many cases, such as with plant growth promoting bacteria and mycorrhizal fungi, whereas a compatible interaction with a parasite or pathogenic microorganism can have drastic negative consequences on plant growth and yield. Root-knot nematodes (RKN) are obligate parasitic worms that invade plant root systems, are able to infest almost all vascular plants and are widespread over most cultivated agricultural regions. We are interested in this intriguing biological phenomena because the success of RKN infection relies on establishing permanent feeding sites within the central vascular cylinder of the root, which is essential for its growth and reproduction. To aid the transfer of plant nutrients, RKN are able to de-differentiate root vascular cells and convert them into specialized nutrient-transfer cells, also known by hematologist as “giant cells”. The ability of RKN to reprogram the development of vascular cells into nutrient-transfer GCs is a fundamental biological question that is still not understood.

Recent studies have shown that the infestation process requires a delicate interaction with plant roots as nematode juveniles enter the root cortex near the elongation zone and first migrate toward the meristem before moving to differentiating vascular cells and molecular analyses have revealed that RKN infection is accompanied by extensive changes in expression of genes involved in cell cycle activation, cell wall modification, hormone and defense. However, the gene expression changes reported for RKN infestation show variable results, bringing into question exactly how these parasitic nematodes can efficiently reprogram differentiated root cells into nutrient-transfer GCs. Research carried out in my group has identified novel signaling components involved in the differentiation of nutrient-transfer cells that are conserved in maize seed (Costa et al., 2012) and in the development of the nutrient-transfer embryonic suspensor in Arabidopsis (Costa et al 2014). We are testing genetically how different genetic pathways regulate RKN infection and in particular in the differentiation of functional nutrient transfer cells at root nematode galls. Our preliminary data suggests that nematodes can efficiently highjack distinct signalling pathways to reprogram root cells into feeding structures.