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

Kan Zhuo,Godelieve Gheysen,Nguyen Xuan Huy,Lander Bauters,Silke Nowak,Diana Naalden

doi:10.1111/mpp.12759

Abstract

SummaryC‐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.

Highlights

Rice is an important crop, providing the staple food for a large part of the world’s population, in Asia
The Mg01965 gene identified from previous work (Haegeman et al, 2013) includes a 681-bp open reading frame (ORF), separated by two introns of 136 and 69 bp
The C-terminal half of the protein contains a C-type lectin (CTL)-like domain (PF00059) from amino acid 51 to amino acid 214, in which there are five key residues that are thought to be involved in carbohydrate binding, and a characteristic C-type lectins (CTLs) motif ‘WIGL’ that is important in forming hydrophobic cores in the tertiary structure of the protein (Bauters et al, 2017) (Figs 1 and S1, see Supporting Information)

Summary

Introduction

Rice is an important crop, providing the staple food for a large part of the world’s population, in Asia. When plants perceive the infection of plant pathogens, a series of immunity responses are activated, such as the mitogen-activated protein kinase signalling cascade and calcium-dependent protein kinase, reactive oxygen species (ROS) burst, deposition of callose, induction of defence-related gene expression and induction of the hypersensitive response (HR) (Asai and Shirasu, 2015; Liu et al, 2012; Zipfel et al, 2004). In RKNs, the effector MiCRT, discovered in Meloidogyne incognita, was the first effector to be confirmed as capable of suppressing the host defence response, including defence-related gene expression and callose deposition, triggered by the PAMP elf (Jaouannet et al, 2013). Several effectors from different RKN species have been demonstrated to function in the suppression of host plant defence and promotion of nematode parasitism. The secreted effector MiMsp from M. incognita suppresses callose deposition, defence-related gene expression and cell death (Niu et al, 2016); the effector MjTTL5 of Meloidogyne javanica can suppress plant innate immunity by activating host ROS-scavenging systems to eliminate ROS (Lin et al, 2016); the effector MeTCTP from Meloidogyne enterolobii suppresses plant immunity by suppressing programmed cell death in host plants (Zhuo et al, 2017)

Results

Discussion

Conclusion