Marie C, Broughton WJ, Deakin WJ (2001) Rhizobium
type III secretion systems: legume charmers or
alarmers? Curr Opin Plant Biol 4(4):336– 342
Masson-Boivin C, Giraud E, Perret X, Batut J (2009)
Establishing nitrogen-fixing symbiosis with legumes:
how manyrhizobiumrecipes? Trends Microbiol 17
(10):458– 466
Murakami E, Nagata M, Shimoda Y, Kucho K-I, Higashi
S, Abe M, Hashimoto M, Uchiumi T (2011) Nitric
Oxide Production Induced in Roots ofLotus japonicus
by Lipopolysaccharide fromMesorhizobium loti. Plant
Cell Physiol 52(4):610– 617
Niwa S, Kawaguchi M, Imazumi-Anraku H, Chechetka
SA, Ishizaka M, Ikuta A, Kouchi H (2001) Responses
of a model legume Lotus japonicusto lipochitin
oligosaccharide nodulation factors purified fromMes-
orhizobium lotiJRL501. Mol Plant Microbe Interact
14(7):848– 856
Nukui N, Minamisawa K, Ayabe S, Aoki T (2006)
Expression of the 1-aminocyclopropane-1-carboxylic
acid deaminase gene requires symbiotic nitrogen-
fixing regulator genenifA2inMesorhizobium loti
MAFF303099. Appl Environ Microbiol 72
(7):4964– 4969
Okazaki S, Zehner S, Hempel J, Lang K, Göttfert M
(2009) Genetic organization and functional analysis of
the type III secretion system of Bradyrhizobium
elkanii. FEMS Microbiol Lett 295(1):88– 95
Okazaki S, Okabe S, Higashi M, Shimoda Y, Sato S,
Tabata S, Hashiguchi M, Akashi R, Göttfert M, Saeki
K (2010) Identification and functional analysis of type
III effector proteins inMesorhizobium loti. Mol Plant
Microbe Interact 23(2):223– 234
Pankhurst CE, Craig AS, Jones WT (1979) Effectiveness
ofLotusroot nodules: I. Morphology andflavolan
content of nodules formed onLotus pedunculatus
by fast growing Lotus rhizobia. J Exp Bot 30
(6):1085– 1093
Pankhurst CE, Hopcroft DH, Jones WT (1987) Compar-
ative morphology andflavolan content ofRhizobium
lotiinduced effective and ineffective root nodules on
Lotusspecies,Leuceana leucocephala,Carmichaelia
flagelliformis, Ornithopus sativus, and Clianthus
puniceus. Can J Bot 65:2676– 2685
Perret X, Staehelin C, Broughton WJ (2000) Molecular
basis of symbiotic promiscuity. Microbiol Mol Biol
Rev 64(1):180– 201
Popendorf K, Tsuyoshi H, Osana Y, Sakakibara Y (2010)
Murasaki: a fast, parallelizable algorithm tofind anchors
from multiple genomes. PLoS One. 5(9):e12651
Pueppke SG, Broughton WJ (1999)Rhizobiumsp. Strain
NGR234 andR. frediiUSDA257 Share Exceptionally
Broad, Nested Host Ranges. Mol Plant Microbe
Interact 12(4):293– 318
Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, RonsonCW
(2006) Excision and transfer of theMesorhizobium
lotiR7A symbiosis island requires an integrase IntS, a
novel recombination directionality factor RdfS, and a
putative relaxase RlxS. Mol Microbiol 62(3):723– 734
Ramsay JP, Sullivan JT, Jambari N, Ortori CA, Heeb S,
Williams P, Barrett DA, Lamont IL, Ronson CW
(2009) A LuxRI-family regulatory system controls
excision and transfer of theMesorhizobium lotistrain
R7A symbiosis island by activating expression of two
conserved hypothetical genes. Mol Microbiol 73
(6):1141– 1155
Ramsay JP, Major AS, Komarovsky VM, Sullivan JT, Dy
RL, Hynes MF, Salmond GP, Ronson CW (2013) A
widely conserved molecular switch controls quorum
sensing and symbiosis island transfer inMesorhizobi-
um lotithrough expression of a novel antiactivator.
Mol Microbiol 87(1):1– 13
Ribbe MW, Hu Y, Guo M, Schmid B, Burgess BK (2002)
The FeMoco-deficient MoFe protein produced by a
nifHdeletion strain ofAzotobacter vinelandiishows
unusual P-cluster features. J Biol Chem 277
(26):23469– 23476
Ritsema T, Wijfjes AH, Lugtenberg BJ, Spaink HP
(1996)Rhizobiumnodulation protein NodA is a host-
specific determinant of the transfer of fatty acids in
Nod factor biosynthesis. Mol Gen Genet 251(1):44– 51
Roche P, Maillet F, Plazanet C, Debelle F, Ferro M,
Truchet G, Prome JC, Denarie J (1996) The common
nodABCgenes ofRhizobium melilotiare host-range
determinants. Proc Natl Acad Sci USA 93(26):
15305 – 15310
Rodpothong P, Sullivan JT, Songsrirote K, Sumpton D,
Cheung KWJT, Thomas-Oates J, Radutoiu S, Stoug-
aard J, Ronson CW (2009) Nodulation Gene Mutants
ofMesorhizobium lotiR7A—nodZandnolLMutants
Have Host-Specific Phenotypes onLotusspp. Mol
Plant Microbe Interact 22(12):1546– 1554
Rohrig H, Schmidt J, Wieneke U, Kondorosi E, Barlier I,
Schell J, John M (1994) Biosynthesis of lipooligosac-
charide nodulation factors:RhizobiumNodA protein is
involved in N-acylation of the chitooligosaccharide
backbone. Proc Natl Acad Sci USA 91(8):3122– 3126
Rubio LM, Ludden PW (2008) Biosynthesis of the iron-
molybdenum cofactor of nitrogenase. Annu Rev
Microbiol 62:93– 111
Sanchez C, Mercante V, Babuin MF, Lepek VC (2012)
Dual effect ofMesorhizobium lotiT3SS functionality
on the symbiotic process. FEMS Microbiol Lett 330
(2):148– 156
Sawada H, Kuykendall LD, Young JM (2003) Changing
concepts in the systematics of bacterial nitrogen-fixing
legume symbionts. J General Appl Microbiol 49
(3):155– 179
Schlaman HR, Phillips DA, Kondorosi E (1998) Genetic
organization and transcriptional regulation of rhizobial
nodulation genes. In: Spaink HP, Kondorosi A,
Hooykaas PJJ (eds) The Rhizobiaceae: Molecular
Biology of Model Plant-Associated Bacteria. Kluwer
Academic Publishers, Dordrecht, pp 361– 386
Schumpp O, Crevecoeur M, Broughton WJ, Deakin WJ
(2009) Delayed maturation of nodules reduces sym-
biotic effectiveness of theLotus japonicus-Rhizobium
sp. NGR234 interaction. J Exp Bot 60(2):581– 59056 K. Saeki and C.W. Ronson