The Lotus japonicus Genome

as nodulation outer proteins (Nops) (Fig.15.1).
Rhizobiumsp. NGR234 secretes at least eight
Nops via the T3SS that are either components of
the T3SS-dependent pilus (NopA and NopB), the
putative translocon that forms pores in the plant
plasma membrane (NopX), or putative effectors
(NopL, NopP, NopJ, NopM, and NopT) (Kambara
et al. 2009 ; Skorpil et al. 2005 ; Saad et al. 2005 ;
Ausmees et al. 2004 ; Viprey et al. 1998 ; Deakin
et al. 2005 ). Among the putative rhizobial effec-
tors, NopL and NopP appear to be specific to rhi-
zobia. Other Nops homologs are widespread in
T3SS-containing pathogens. NopJ, for example,
belongs to the YopJ family of ubiquitin-like pro-
tein proteases found in many plant and animal
pathogens. This family includes numerous Avr
proteins such as AvrBsT ofXanthomonas cam-
pestrispv.vesicatoria, a pathogen ofVignaand
soybean (Marie et al. 2003 ). NopM is homologous
to YopM ofYersinia pestis. YopM is a nuclear-
targeting protein that modulates phosphorylation
signaling cascades and diminishes defense
responses in animal cells (Viboud and Bliska
2005 ). NopT has homology with the Avr protein
AvrPphB of the phytopathogen Pseudomonas
syringaeas well as YopT ofYersiniaspp. (Shao
et al. 2003 ). Proteins of this family are cysteine

proteases. The proteolytic activity of AvrPphB is

essential for autoproteolytic cleavage of an Av-

rPphB precursor as well as for eliciting the

hypersensitive response (HR) in plants. The

effector repertoires vary in size and composition

between strains, which might determine the host-

dependent effect of T3SS.

Host legume gene expression affected by

rhizobial T3SS has recently been elucidated.

Sánchez et al. reported that the relative expres-

sion levels of gibberellin-2 oxidase (GA-2 OXI-

DASE), flavanone 3-hydroxylase (F3H), and

nodule inception (NIN) inL. japnonicuswere

significantly reduced in roots inoculated with the

T3SS mutant compared to those inoculated with

the wild-type strain of M. loti MAFF303099

(Sánchez et al. 2009 ). The GA-2 OXIDASE and

F3H genes are strongly induced in mature nod-

ules (Kouchi et al. 2010 ), while the NIN gene,

after induction by Nod factors (Schauser et al.

1999 ), maintains and increases its expression

during nodulation. Bartsev et al. ( 2004 ) reported

that ectopic expression of rhizobial effector gene

nopLinL. japonicussuppressed the expression

of pathogen-related (PR) genes, chitinase, and

glucanase (Bartsev et al. 2004 ). Biochemical

studies revealed that NopL is a substrate for plant

Fig. 15.1 Nodulation signaling and modulation by the
rhizobial type III secretion system. A host plant-derived
flavonoid induces the production of Nod factors (NFs) in
rhizobia. Recognition of NFs by NF receptors (NFRs)
triggers a signaling cascade leading to nodulation. The

flavonoid also induces rhizobial T3SS, which injects

effector proteins into host cells. One effector modulates

nodulation signaling toward nodulation, whereas another

is recognized by the host defense system, which is capable

of aborting the nodulation process

166 T. Nakagawa et al.