Plant-parasitic nematodes (PPNs) are a large group of obligate biotrophic pathogens that secrete molecules, called effectors, involved in parasitism. The majority of work in molecular phytonematology has focused on the root-knot and cyst nematodes, which are both sedentary endoparasitic nematodes. More recently, inexpensive sequencing technology has facilitated effector searches in PPNs with different parasitic lifestyles. Work in different PPN species suggests that effectors are diverse, and selection pressure from plant hosts has contributed to the presence of large, expanded effector gene families. The identification of promoter elements/motifs preceding effector gene sequences suggests that promoter analysis can computationally predict new putative effectors. However, until a method of genetic transformation is available for PPNs, work on characterizing effectors will be hindered.

Root-knot nematodes (RKNs; Meloidogyne spp.) engage in complex parasitic interactions with many different host plants around the world, initiating elaborate feeding sites and disrupting host root architecture. Although RKNs have been the focus of research for many decades, new molecular tools have provided useful insights into the biological mechanisms these pests use to infect and manipulate their hosts. From identifying host defense mechanisms underlying resistance to RKNs to characterizing nematode effectors that alter host cellular functions, the past decade of research has significantly expanded our understanding of RKN–plant interactions, and the increasing number of quality parasite and host genomes promises to enhance future research efforts into RKNs. In this review, we have highlighted recent discoveries, summarized the current understanding within the field, and provided links to new and useful resources for researchers. Our goal is to offer insights and tools to support the study of molecular RKN–plant interactions.

Jasmonic acid (JA) is a plant hormone that plays important roles in regulating plant defenses against necrotrophic pathogens and herbivorous insects, but the role of JA in mediating the plant responses to root-knot nematodes has been unclear. Here we show that an application of either methyl jasmonate (MeJA) or the JA-mimic coronatine (COR) on Arabidopsis significantly reduced the number of galls caused by the root-knot nematode Meloidogyne hapla. Interestingly, the MeJA-induced resistance was independent of the JA-receptor COI1 (CORONATINE INSENSITIVE 1). The MeJA-treated plants accumulated the JA precursor cis-(+)-12-oxo-phytodienoic acid (OPDA) in addition to JA/JA-Isoleucine, indicating a positive feedback loop in JA biosynthesis. Using mutants in the JA-biosynthetic pathway, we found that plants deficient in the biosynthesis of JA and OPDA were hyper-susceptible to M. hapla. However, the opr3 mutant, which cannot convert OPDA to JA, exhibited wild-type levels of nematode galling. In addition, mutants in the JA-biosynthesis and perception which lie downstream of opr3 also displayed wild-type levels of galling. The data puts OPR3 (OPDA reductase 3) as the branch point between hyper-susceptibility and wild-type like levels of disease. Overall, the data suggests that the JA precursor, OPDA, plays a role in regulating plant defense against nematodes.

Root-knot nematodes secrete effectors that manipulate their host plant cells so that the nematode can successfully establish feeding sites and complete its lifecycle. The root-knot nematode feeding structures, their “giant cells,” undergo extensive cytoskeletal remodeling. Previous cytological studies have shown the cytoplasmic actin within the feeding sites looks diffuse. In an effort to study root-knot nematode effectors that are involved in giant cell organogenesis, we have identified a nematode effector called MiPFN3 (Meloidogyne incognita Profilin 3). MiPFN3 is transcriptionally up-regulated in the juvenile stage of the nematode. In situ hybridization experiments showed that MiPFN3 transcribed in the nematode subventral glands, where it can be secreted by the nematode stylet into the plant. Moreover, Arabidopsis plants that heterologously expressed MiPFN3 were more susceptible to root-knot nematodes, indicating that MiPFN3 promotes nematode parasitism. Since profilin proteins can bind and sequester actin monomers, we investigated the function of MiPFN3 in relation to actin. Our results show that MiPFN3 suppressed the aberrant plant growth phenotype caused by the misexpression of reproductive actin (AtACT1) in transgenic plants. In addition, it disrupted actin polymerization in an in vitro assay, and it reduced the filamentous actin network when expressed in Arabidopsis protoplasts. Over a decade ago, cytological studies showed that the cytoplasmic actin within nematode giant cells looked fragmented. Here we provide the first evidence that the nematode is secreting an effector that has significant, direct effects on the plant’s actin cytoskeleton. Root-knot nematodes are microscopic plant pests that infect plant roots and significantly reduce yields of many crop plants. The nematodes enter the plant roots and modify plant cells into complex, multinuclear feeding sites called giant cells. The formation and maintenance of giant cells is critical to nematode survival. During giant cell organogenesis, the progenitor plant cells undergo many morphological changes, including a re-organization of the cytoplasmic actin cytoskeleton. As a result, the giant cell cytoplasmic actin appears fragmented and disorganized. Plant cells can regulate their actin filament assembly, in part, through the expression of actin binding proteins such as profilins. Here we show that infectious nematode juveniles express a profilin called MiPFN3. Expression of MiPFN3 in Arabidopsis plants made the plants more susceptible to root-knot nematodes, indicating that MiPFN3 acts as an effector that aids parasitism. We show evidence that the expression MiPFN3 in plant cells causes the fragmentation of plant actin filaments. The work here demonstrates that nematode effector MiPFN3 can directly affect plant actin filaments, whose reorganization is necessary for giant cell formation.

Root-knot and cyst nematodes are two groups of plant parasitic nematodes that cause the majority of crop losses in agriculture. As a result, these nematodes are the focus of most nematode effector research. Root-knot and cyst nematode effectors are defined as secreted molecules, typically proteins, with crucial roles in nematode parasitism. There are likely hundreds of secreted effector molecules exuded through the nematode stylet into the plant. The current research has shown that nematode effectors can target a variety of host proteins and have impacts that include the suppression of plant immune responses and the manipulation of host hormone signaling. The discovery of effectors that localize to the nucleus indicates that the nematodes can directly modulate host gene expression for cellular reprogramming during feeding site formation. In addition, plant peptide mimicry by some nematode effectors highlights the sophisticated strategies the nematodes employ to manipulate host processes. Here we describe research on the interactions between nematode effectors and host proteins that will provide insights into the molecular mechanisms underpinning plant–nematode interactions. By identifying the host proteins and pathways that are targeted by root-knot and cyst nematode effectors, scientists can gain a better understanding of how nematodes establish feeding sites and subvert plant immune responses. Such information will be invaluable for future engineering of nematode-resistant crops, ultimately fostering advancements in agricultural practices and crop protection. [ ] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 “No Rights Reserved” license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2024.