Disparate role of rhizobial ACC deaminase in root-nodule symbioses

Symbiosis

Valérie Murset • Hauke Hennecke • Gabriella Pessi

V. Murset()

ETH Zürich, Institute of Microbiology,

Wolfgang-Pauli-Strasse 10,
8093 Zürich, Switzerland

e-mail:

Online Resource 1List of members of the Rhizobiales which contain an acdS-like gene based on a database search using theB. japonicum blr0241 gene as a query sequence (n.a., not available or not applicable)

Members of the Rhizobiales with annotated ACC deaminase genes / Relevant additional information / References
Bradyrhizobium japonicum USDA 110 / Insertion mutant of blr0241 has no nodulation deficiency in symbiosis with siratro, cowpea, mungbean and soybean. As competitive as the wild-type strain in symbiosis with soybean. / This work
Bradyrhizobium sp. / n.a. / n.a.
Burkholderia phymatum,
Burkholderia tuberum / ACC deaminase activity was measured. / Onofre-Lemus et al. 2009
Mesorhizobium loti MAFF303099 / Insertion mutant of acdS has decreased ability to nodulate L. japonicus MG20. Less competitive in nodulation than the wild-type strain. Mutant constitutively expressing the acdS gene induces formation of more nodules and is more competitive than the wild-type strain in L. japonicus and L. tenuis nodulation. / Uchiumi et al. 2004; Conforte et al. 2010
Mesorhizobium ciceri, Mesorhizobium loti R7A, Mesorhizobium opportunistum WSM2075 / n.a. / n.a.
Rhizobium leguminosarum bv. viciae / Insertion mutant in Rhizobium leguminosarum bv. viciae acdS causes decreased nodule number compared to the wild type in symbiosis with Pisum sativum L. cv. Sparkle. Mutant overexpressing AcdS shows same behavior as the wild type in symbiosis with Pisum sativum L. cv. Sparkle. The acdS gene of R. leguminosarum bv. viciae introduced in S. meliloti results in strain with 35 to 40% greater efficiency in nodulating Medicago sativa and more competitiveness in nodulation. / Ma et al. 2003,
Ma et al. 2004
Rhizobium sp. strain TAL1145 / Introduction of a multicopy plasmid with Rhizobium sp. strain TAL1145 acdS leads toincreased nodule number, nodule dry weight and root dry weight in symbiosis with Leucaena leucocephalacompared to the wild type. / Tittabutr et al. 2008
Rhizobium gallicum, Rhizobium leguminosarum bv. phaseoli, Rhizobium leguminosarum bv. trifolii, Rhizobium sullae / n.a. / n.a.
Sinorhizobium sp. strain BL3 / acdS from Sinorhizobium sp. BL3 cloned in Rhizobium sp. strain TAL1145 leads to increase of the bacterial ACC deaminase activity and enhanced symbiotic efficiency (greater number and size of nodules) on L. leucocephala. / Tittabutr et al. 2008
Sinorhizobium medicae, Sinorhizobium meliloti / n.a. / n.a.
Agrobacterium tumefaciens D3 / ACC deaminase activity was measured. Double mutant ofacdS and lrpL yields smaller canola seedlings root length compared to seedlings inoculated with the wild type, but there was no difference in the ability of inhibiting crown gall development induced by A. tumefaciens C58. / Hao et al. 2011
Agrobacterium radiobacter K84, Agrobacterium vitis S4 / n.a. / n.a.
Azorhizobium caulinodans ORS 571 / n.a. / n.a.
Methylobacterium fujisawaense / ACC deaminase activity was measured. Lower amount of ACC was detected in the canola seedling treated with M. fujisawaense. / Madhaiyan et al. 2006
Methylobacterium oryzae / Can use ACC as nitrogen source. Lower amount of ACC was detected in root exudates of canola treated with M. oryzae. / Madhaiyan et al. 2007
Methylobacterium chloromethanicum CM4, Methylobacterium extorquens, Methylobacterium nodulans ORS 2060, Methylobacterium radiotolerans, Methylobacterium sp. / n.a. / n.a.
Parvibaculum lavamentivorans DS-1 / n.a. / n.a.
Phyllobacterium brassicacearum / n.a. / n.a.
Pseudomonas putida UW4 / acdS fromP. putida UW4 introduced in A. tumefaciens leads to inhibition of tumor formation on tomato and castor bean plant, the reduction of ethylene production by plant tissues during the infection process, and it increases the transformation efficiency of canola. / Hao et al. 2007, Hao et al. 2010
Pseudomonas sp. strain ACP / acdS from Pseudomonas sp. strain ACP introduced in A. tumefaciens C58 leads to a reduced ethylene production of infected melon cotyledons and increases the A. tumefaciens-mediated transformation ability. / Nonaka et al. 2008
Pseudomonas brassicacearum, Pseudomonas entomophila, Pseudomonas fluorescens, Pseudomonas plecoglossicida, Pseudomonas stutzeri, Pseudomonas syringae, Pseudomonas tolaasii / n.a. / n.a.
Rhodopseudomonas palustris BisA53 / n.a. / n.a.

Online Resource 2 Expression profile of the B. japonicum blr0241 gene and its protein product revealed by transcriptomics and proteomics (n.t., not tested)

Conditions for the wild type / Transcriptomics1
(fold-change relative to aerobically grown wild type) / Proteomics2
(spectral counts)
free-living
in micro-oxic culture / 4.8 / n.t.
in anoxic culture / 12.2 / n.t.
symbiotic
in soybean nodules / 20.1 / 853
in mungbean nodules / 23.7 / n.t.
in siratro nodules / 14.6 / 477
in cowpea nodules / 17.2 / 527

1Data extracted from Pessi et al. (2007) and Koch et al. (2010)

2Data extracted from Delmotte et al. (2010) and Koch et al. (2010)

Online Resource data references:

Conforte VP, Echeverria M, Sanchez C, Ugalde RA, Menendez AB, Lepek VC (2010) Engineered ACC deaminase-expressing free-living cells of Mesorhizobium loti show increased nodulation efficiency and competitiveness on Lotus spp. J Gen Appl Microbiol 56:331-338.

Delmotte N, Ahrens CH, Knief C, Qeli E, Koch M, Fischer HM, Vorholt JA, Hennecke H, Pessi G (2010) An integrated proteomics and transcriptomics reference data set provides new insights into the Bradyrhizobium japonicum bacteroid metabolism in soybean root nodules. Proteomics 10:1391-1400.

Hao Y, Charles TC, Glick BR (2007) ACC deaminase from plant growth-promoting bacteria affects crown gall development. Can J Microbiol 53:1291-1299.

Hao Y, Charles TC, Glick BR (2010) ACC deaminase increases the Agrobacterium tumefaciens-mediated transformation frequency of commercial canola cultivars. FEMS Microbiol Lett 307:185-190.

Hao Y, Charles TC, Glick BR (2011) ACC deaminase activity in avirulent Agrobacterium tumefaciens D3. Can J Microbiol 57:278-286.

Koch M, Delmotte N, Rehrauer H, Vorholt JA, Pessi G, Hennecke H (2010) Rhizobial adaptation to hosts, a new facet in the legume root-nodule symbiosis. Mol-Plant Microbe Interact 23:784-790.

Ma WB, Guinel FC, Glick BR (2003) Rhizobium leguminosarum bv. viciae 1-aminocyclopropane-1 carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69:4396-4402.

Ma WB, Charles TC, Glick BR (2004) PV expression of an exogenous 1-aminocyclopropane 1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891-5897.

Madhaiyan M, Poonguzhali S, Ryu JH, Sa TM (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense.Planta 224:268-278.

Madhaiyan M, Kim BY, Poonguzhali S, Kwon SW, Song MH, Ryu JH, Go SJ,Koo BS, Sa TM (2007)Methylobacterium oryzae sp. nov., an aerobic, pink-pigmented, facultatively methylotrophic, 1 aminocyclopropane-1-carboxylate deaminase-producing bacterium isolated from rice. Int J Syst Evol Micr 57:326-331.

Nonaka S, Sugawara M, Minamisawa K, Yuhashi K, Ezura H (2008) 1-aminocyclopropane-1-carboxylatedeaminase enhances Agrobacterium tumefaciens-mediated gene transfer into plant cells. Appl Environ Microbiol 74:2526-2528.

Onofre-Lemus J, Hernández-Lucas I, Girard L, Caballero-Mellado J (2009) ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl Environ Microbiol 75:6581-6590.

Pessi G, Ahrens CH, Rehrauer H, Lindemann A, Hauser F, Fischer HM, Hennecke H (2007) Genome-wide transcript analysis of Bradyrhizobium japonicum bacteroids in soybean root nodules. Mol Plant-Microbe Interact 20:1353-1363.

Tittabutr P, Awaya JD, Li QX, Borthakur D (2008) The cloned 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene from Sinorhizobium sp. strain BL3 in Rhizobium sp. strain TAL1145 promotes nodulation and growth of Leucaena leucocephala. System Appl Microbiol 31:141-150.

Uchiumi T, Ohwada T, Itakura M, Mitsui H, Nukui N, Dawadi P, Kaneko T, Tabata S, Yokoyama T, Tejima K, Saeki K, Omori H, Hayashi M, Maekawa T, Sriprang R, Murooka Y, Tajima S, Simomura K, Nomura M, Suzuki A, Shimoda Y, Sioya K, Abe M, Minamisawa K (2004) Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J Bacteriol 186:2439-2448.

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