A Meloidogyne graminicola C‐type lectin, Mg01965, is secreted into the host apoplast to suppress plant defence and promote parasitism

Abstract

Summary C‐type lectins (CTLs), a class of multifunctional proteins, are numerous in nematodes. One CTL gene, Mg01965 , shown to be expressed in the subventral glands, especially in the second‐stage juveniles of the root‐knot nematode Meloidogyne graminicola , was further analysed in this study. In vitro RNA interference targeting Mg01965 in the preparasitic juveniles significantly reduced their ability to infect host plant roots. Immunolocalizations showed that Mg01965 is secreted by M. graminicola into the roots during the early parasitic stages and accumulates in the apoplast. Transient expression of Mg01965 in Nicotiana benthamiana and targeting it to the apoplast suppressed the burst of reactive oxygen species triggered by flg22. The CTL Mg01965 suppresses plant innate immunity in the host apoplast, promoting nematode parasitism in the early infection stages.

Analyses of the Root-Knot Nematode (Meloidogyne graminicola) Transcriptome during Host Infection Highlight Specific Gene Expression Profiling in Resistant Rice Plants

“…Our comparative transcriptomic data also showed that M. graminicola relies on the secretion of a set of effector proteins, in addition to CWDEs or peptidases, to establish infection within rice, whether susceptible or resistant cultivars. Effectors are produced by pathogens to facilitate parasitism and a small amount of M. graminicola secreted proteins have been described [ 11 , 12 , 13 , 14 , 15 ]. Mining the M. graminicola transcriptome returned eight novel candidate effectors in addition to those previously described in Petitot et al [ 10 ].…”

“…Like MgPDI and Me-TCTP , MgGPP is another effector that may be involved in the suppression of defense reactions of the host cell to promote parasitism [ 11 ]. Among the M. graminicola genes highly expressed in pre-J2s, Mg448 encodes a C-type lectin that could also be involved in overcoming the host defenses as reported for Mg01965 [ 14 ] and for the cyst nematode, Heterodera glycines [ 53 ].…”

“…In the rice– M. graminicola -compatible interaction, nematode effectors were identified from comprehensive transcriptomic analyses of pre-parasitic J2s and rice infected tissues [ 9 , 10 ], spanning from J2 penetration to development into young adult females (from 2 to 16 dpi) [ 10 ]. Over the past years, novel M. graminicola effectors playing a role in nematode parasitism were functionally characterized, including pioneer genes [ 11 , 12 , 13 ], a C-type lectin [ 14 ], and a protein disulfide isomerase (PDI) [ 15 ]. Several RKN effectors characterized so far on tomato or Arabidopsis thaliana are able to interact with host proteins and consequently can interfere with cellular processes within the plant cell or in the apoplast to facilitate nematode infection (for review [ 6 ]).…”

Role of Protein Glycosylation in Host-Pathogen Interaction

“…The lectin calreticulin [210,211] Mi-CRT secreted by Meloidogyne incognita [212] can inhibit the PAMP-triggered immunity (PTI) elicited by ELF18 that derives from the N-terminal of bacterial elongation factor-Tu. The C-type lectin Mg01965 secreted by M. graminicola can suppress the PTI induced by flg22 which is a PAMP from the N-terminal of bacterial flagellin [131]. The above two lectins are unlikely to mask oligosaccharides, since carbohydrate residues are absent in ELF18 and flg22.…”

Plant defense responses in monocotyledonous and dicotyledonous host plants during root-knot nematode infection

“…Interesting results were also obtained for RKN lectin, which was experimentally demonstrated to be secreted into host plants as an effector, e.g., Mg01965 from M. graminicola. This protein is released during the early stages of infection and accumulates in the apoplast, where it can suppress PTI, possibly by binding to certain apoplastic sugars and by interfering with sugar signals (Zhuo et al 2019). Effector proteins can also be conserved between some economically important Meloidogyne species, such as M. hapla, M. incognita, and M. graminicola, as described in the example of the Msp18 protein (Grossi-de-Sa et al 2019).…”