functionally distinct from that of NFR1 because
the chimeric gene consisting of the LysM domain
of NFR1 and the kinase domain of AtCERK1 did
not rescue the symbiotic defect ofLotus nfr1
mutants (Nakagawa et al. 2011 ). Surprisingly,
however, only three consecutive amino acid
substitutions in the AtCERK1 kinase domain
conferred the symbiotic activity to the chimeric
receptor. In addition to the structural similarity
between chitin oligosaccharides and NFs, these
findings suggest the close evolutionary relation-
ships between defense and symbiosis.
15.3 Pathogenic Aspect of the
Symbiotic Partner
Rhizobia are beneficial to the host plants; how-
ever, their family,Rhizobiaceae, also includes a
pathogenic microbe,Agrobacterium. The patho-
genic strains of Rhizobiaceae carry virulence
genes as plasmids named pTi or pRi that are
required for tumorigenic or hairy root-inducing
symptoms, respectively. On the other hand, in
symbiotic strains, the genera Rhizobium and
Sinorhizobiumcarry plasmids (pSym) containing
nodandnifgenes that are indispensable for the
nodulation and nitrogenfixation (see Chap. 6 ).
Therefore, these plasmids are the critical deter-
minants for pathogenic or symbiotic phenotypes.
Interestingly, these plasmids are transferred
among pathogenic, nonpathogenic, and symbi-
otic species (Chen et al. 2001 ; Moulin et al.
2001 ; Vandamme et al. 2002 ). In addition, nat-
ural strains carrying pTi, pRi, and pSym together
were found and confirmed to have the ability for
inducing tumors, hairy roots, and nodules (Ve-
lazquez et al. 2005 ).
As mentioned in Chap. 6 , rhizobia also carry a
set of genes for the T3/4SS in the symbiosis
islands or sym plasmids. The genes encoding
T3SSs have been found not in all, but in some
rhizobia including Rhizobium sp. NGR234,
Sinorhizobium fredii, Bradyrhizobium japoni-
cum, B. elkanii, and Mesorhizobium loti
MAFF303099, whereasM. lotiR7A possesses
T4SS (Deakin and Broughton 2009 ). A distinc-
tive feature of rhizobial secretion systems is that
the expression is tightly regulated byflavonoids
derived from the host legume. This unique reg-
ulation is achieved by the transcriptional regu-
lator NodD which senses the hostflavonoids and
activates genes downstream of special promoters
callednodboxes (Spaink 1995 ) (see Chap. 6 ).
The nod boxes are found not only in the
upstream of genes for Nod-factor synthesis (e.g.,
nod, noe, and nol), but also in the promoter
region of the transcriptional activatorttsI. TtsI
activates transcription of T3SS genes by binding
to specific cis-elements (tts boxes) found
upstream of the rhizobial T3SS genes (Krause
et al. 2002 ). Therefore, the activation of T3SS
appears to be coordinated with the biosynthesis
of Nod factors, which initiate nodule organo-
genesis in host legumes.15.4 Physiological Roles of
Rhizobial Type III Secretion
System and EffectorsDepending on the host plant species, rhizobial
T3SS approaches result in different effects. InM.
lotiMAFF303099, for example, deletion oftts
genes led to a reduced nodule number withLotus
corniculatus subsp. frondosus (Okazaki et al.
2010 ). Likewise, deletion ofB. japonicum tts
genes caused a reduction in nodule number on
Macroptilium atropurpureumand delayed nod-
ulation with soybean (Krause et al. 2002 ). Sim-
ilar nodulation enhancement has also been
observed in other T3SS-containing rhizobia. The
infection and nodulation processes that the rhi-
zobial T3SS facilitates remain to be elucidated.
However, transcriptional studies have shown that
rhizobial T3SS is expressed at all stages of
infection. The T3SS ofB. japonicumUSDA110
was expressed in infection threads and develop-
ing nodules ofGlycine max(Zehner et al. 2008 ),
and expression of several T3SS genes ofRhizo-
biumsp. NGR234 was detected in mature nod-
ules ofCajanus cajanandV. unguiculata(Perret
et al. 1999 ; Viprey et al. 1998 ).
In pathogenic microbes, T3/4SS is a delivery
system of virulence agents, i.e., effector proteins.
In rhizobia, these secreted proteins are designated15 Genes Involved in Pathogenesis... 165