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 put 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.

ML (MD2-related lipid recognition) proteins are known to enhance innate immune responses in mammals. This study reports the analysis of the putative ML gene family in Arabidopsis thaliana and suggests a role for the ML3 gene in herbivory-associated responses in plants. Feeding by larvae of the Lepidopteran generalist herbivore Spodoptera littoralis and larvae of the specialist herbivore Plutella xylostella activated ML3 transcription in leaf tissues. ML3 loss-of-function Arabidopsis plants were compromised in the upregulation of herbivory-induced genes and displayed a semi-dwarf phenotype. Herbivory bioassays showed that larvae of S. littoralis fed on ml3 mutant plants gained more weight compared to larvae fed on wild-type plants while larvae of P. xylostella did not show any significant difference. Virus-induced gene silencing of ML3 expression in plants compromised in jasmonic acid (JA) and salicylic acid (SA) signalling revealed a complex role of ML3 in JA/defence signalling affecting both JA- and SA-dependent responses. The data suggest that ML3 is involved in herbivory-mediated responses in Arabidopsis and that it has a potential role in herbivory-associated molecular pattern recognition.

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