“Cyst-ained” research into Heterodera parasitism

Nematodes are roundworms that constitute the phylum Nematoda. Only a small fraction of nematode genera contains plant-parasitic or animal-parasitic species, while the majority of nematodes are free-living [1]. Heterodera glycines, the soybean cyst nematode, is a plant-parasitic nematode causing major damage to soybean production worldwide. Annual United States yield loss estimates due to H. glycines range up to $1.2 billion, likely making this nematode the most serious pathogen threat to sustainable soybean production [2]. While cyst nematoderesistant soybean cultivars are available, they do not control all H. glycines biotypes present in a given field and, therefore, select for virulent nematode populations that can overcome available resistance genes, leading to a slow but steady erosion of resistance efficacy [3]. Clearly, longterm management of the soybean cyst nematode in modern soybean production will need additional tools, and it is likely that such new tools will be developed from detailed molecular knowledge of the complex Heterodera cyst nematode-plant interactions. This short review provides a snapshot of currently unfolding research discoveries from the genus Heterodera, which also includes other cyst nematodes, particularly the sugar beet cyst nematode H. schachtii, which can infect Arabidopsis and therefore has been used as a model system. Since nematode effectors (the proteins delivered into host plant tissues to mediate parasitism) are at the forefront of nematode–plant interactions, their identification and functional characterization are heavily emphasized in this manuscript. Heterodera cyst nematodes are soil-borne pathogens. Infective juveniles (Fig 1A) hatch from eggs that are mostly contained in the hardened body wall of the previous generation’s female, which represents the cyst structure giving this nematode group its name (Fig 1B). Infective juveniles migrate toward roots of host plants and penetrate intracellularly into and through the root tissue using mechanical force and cell wall-degrading enzymes delivered through a hollow mouth spear: the stylet (Fig 1A). Interestingly, during their intracellular migration toward the root’s central cylinder, nematodes do not feed but select an initial feeding cell only at the end of their migration, when they become sedentary. At this point, the cyst nematode–plant interactions enter into a new, complex molecular phase of signal exchange, at the end of which the nematode will have reprogrammed a group of several hundred root cells to redifferentiate, partially dissolve their cell walls, and fuse to form a feeding structure: the syncytium (Fig 1C). This new plant organ is the evolutionary advancement that enabled the sedentary parasitic lifestyle of cyst nematodes, as the growing cyst nematodes now require intense levels of nourishment in one single location without the nematodes’ ability to move to new food sources. This also means that a cyst nematode’s survival and reproduction is tightly linked to the proper development and function of the syncytium. At the heart of syncytium induction and formation are signals sent by the nematode to the initial feeding cell, and the most obvious candidates for such signals are effector proteins