MAP kinase, suggesting that NopL modulates
signaling pathways that culminate in the activa-
tion of PR genes. Therefore, these effector pro-
teins should play positive roles for the rhizobial
infection.
In plant–pathogen interactions, a secretion of
the effecter proteins to incompatible host plants is
perceived by NB-LRR receptors and results in
the induction of ETI and thus has a detrimental
effect to the pathogenicity. From these results,
effectors were sometimes called “avirulence
gene”(Avr). Similar results were also observed
in rhizobial infections. InLotus halophilus, for
example, the wild-type strain of M. loti
MAFF303099 almost completely retards nodule
formation, while the number of nodules drasti-
cally increases when inoculated with a T3SS null
mutant. In this interaction, a gene ofM. loti
mlr6361 was identified as the major determinant
of the nodulation restriction. The predicted gene
product of mlr6361 is a protein of 3,056 amino
acids containing 15 repetitions of a sequence
motif of 40–45 residues and a shikimate kinase-
like domain at its carboxyl terminus. Homologs
with similar repeat sequences are present in the
hypersensitive response and pathogenicity (Hrp)
regions of several plant pathogens, including
strains ofP. syringae,Ralstonia solanacearum,
andXanthomonasspecies. These results suggest
thatL. halophilusrecognizes Mlr6361 as poten-
tially pathogen derived, and subsequently halts
the infection process. Similar negative (Avr-like)
effects on the nodulation of legumes have been
reported in several other cases such as NopJ and
NopT of NGR234 inP. vulgarisandC. juncea,
respectively. In most incompatible interactions,
nodulation of the T3SS-harboring strain is com-
pletely abolished, indicative of the involvement
of a rapid and robust defense reaction, which is
reminiscent of ETI. Considering the homology of
Nops to Avr proteins of phytopathogens, it is
tempting to speculate that these Nops are rec-
ognized by the leguminous R genes.
Although the detailed analyses ofLotus R
genes are missing, the symbiotic function of R
gene has recently been elucidated in soybean. In
general, soybeans establish a mutualistic symbi-
osis with wide range of rhizobia including genus
Bradyrhizobium or Sinorhizobium. However,
some soybean cultivars belonging toRj2,Rj3,
Rj4,orRfg1restrict the symbiotic partner to the
specific strains ofBradyrhizobium(Hayashi et al.
2012 ) andSinorhizobium. Among them, soybean
cultivar Hardee, which carriesRj2,formed no
nodules in the inoculation of USDA122, while
other strains such as USDA110 induced forma-
tion of fully matured nodules. Yang et al. ( 2010 )
revealed that the soybeanRj2encodes the Toll-
interleukin receptor/nucleotide-binding site/leu-
cine-rich repeat (TIR-NBS-LRR) class of plant R
protein. In addition, T3SS mutants of USDA122
that abolish the secretion of typical effector pro-
teins gained the ability to nodulate Hardee
(Tsukui et al. 2013 ). These results suggest the
Avr–R interaction governs host specificity of
nodulation between rhizobia and legumes
includingLotusspp. The involvement of legume
R genes in the control of genotype-specific
nodulation reveals a common recognition
mechanism underlying symbiotic and pathogenic
host–bacteria interactions.15.5 Candidates of the Model
Pathogen inL. japonicusAlthough there are some reports of fungal and
bacterial diseases (Sisterna and Lori 2005 ; Alippi
2005 ), only a few inoculation systems were
reported forL. japonicus(Schumpp et al. 2007 ;
Takeuchi et al. 2007 ). For example, Schumpp et al.
( 2007 ) have performed the inoculation tests on
severalLotusspecies with various kinds of viruses
that are known to infect legumes such asMedicago
sativa,orTrifolium pratense. However, these
Lotusplants were resistant to almost all tested
viruses and only specific isolates ofAlfalfa mosaic
virusandTobacco ringspot viruswere able to
infect occasionally. After the adaptation of these
viruses, highly virulent inoculum of Alfalfa
mosaic virus to Lotus plants was obtained
(Schumpp et al. 2007 ). Because the susceptibility
to the obtained virus varied among the different
Lotus accessions or species, this pathosystem
seems to be a good model for analyzing the genes
involved in the virus resistance in legumes.15 Genes Involved in Pathogenesis... 167