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Azospirillum Brasilense and Azospirillum Lipoferum Hydrolyze Conjugates of GA20 and Metabolize the Resultant Aglycones to GA1 in Seedlings of Rice Dwarf Mutants1

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Azospirillum Brasilense and Azospirillum Lipoferum Hydrolyze Conjugates of GA20 and Metabolize the Resultant Aglycones to GA1 in Seedlings of Rice Dwarf Mutants1 Azospirillum brasilense and Azospirillum lipoferum Hydrolyze Conjugates of GA20 and Metabolize the Resultant Aglycones to GA1 in Seedlings of Rice Dwarf Mutants1 Fabricio Cassa´n, Rube´n Bottini*, Gernot Schneider, and Patricia Piccoli Laboratorio de Fisiologı´a Vegetal, Departamento de Ciencias Naturales, Universidad Nacional de Rı´o Cuarto, Campus Universitario, 5800 Rı´o Cuarto, Argentina (F.C., R.B., P.P.); and Leibniz Institut fu¨r Pflanzenbiochemie, Weinberg 3, 0261 Halle, Saale, Germany (G.S.) Azospirillum species are plant growth-promotive bacteria whose beneficial effects have been postulated to be partially due to production of phytohormones, including gibberellins (GAs). In this work, Azospirillum brasilense strain Cd and Azo- spirillum lipoferum strain USA 5b promoted sheath elongation growth of two single gene GA-deficient dwarf rice (Oryza 2 sativa) mutants, dy and dx, when the inoculated seedlings were supplied with [17,17- H2]GA20-glucosyl ester or [17,17- 2 H2]GA20-glucosyl ether. Results of capillary gas chromatography-mass spectrometry analysis show that this growth was 2 ␤ 2 due primarily to release of the aglycone [17,17- H2]GA20 and its subsequent 3 -hydroxylation to [17,17- H2]GA1 by the microorganism for the dy mutant, and by both the rice plant and microorganism for the dx mutant. Azospirillum spp. are considered to be important almost exclusively with Glc, either via the carboxyl plant growth promotive rhizobacteria that can im- group forming glucosyl esters or via the hydroxyl prove the growth and yield of at least several plant group generating glucosyl ethers in a range of iso- species (Okon and Labandera-Gonza´lez, 1994). How- meric forms. These glucosyl conjugates do not ap- ever, the mechanism by which Azospirillum spp. and pear to be biologically active per se; rather, their role other promotive rhizobacteria promote plant growth is proposed to be as reserve, transport, or entry to has yet to be elucidated (Glick et al., 1999, and liter- catabolism forms (Schneider and Schliemann, 1994). ature cited therein). Phytohormone production (Tien GA production in vitro by Azospirillum spp. and et al., 1979; Okon and Kapulnik, 1986), including the effects of Azospirillum spp. on infected plants gibberellins (GAs; Bottini et al., 1989; Fulchieri et al., have been studied earlier. Thus, GA1 and GA3 were 1993; Lucangeli and Bottini, 1997), is one mechanism characterized by capillary gas chromatography-mass that has been proposed. spectrometry (GC-MS) from gnotobiotic cultures of GAs are a class of phytohormones with many dem- Azospirillum lipoferum (Bottini et al., 1989) and Azos- onstrated effects on a number of physiological pro- pirillum brasilense (Janzen et al., 1992). In addition, the cesses (Davies, 1995). Among the 130 GAs identified bacteria have also been shown to metabolize exoge- nous GAs (Piccoli and Bottini, 1994; Piccoli et al., up to now from plants, fungi, and bacteria are GA1, GA , and GA , the three most common directly ef- 1996). External factors such as light quality (Piccoli 3 4 and Bottini, 1996) or oxygen availability and osmotic fective GA shoot elongation promoters. Their levels strength (Piccoli et al., 1999) may also influence the in plant tissues appear to be regulated by three pro- amount and type of GA produced. It was also found cesses: (a) biosynthesis, (b) reversible conjugation, that application of GA in concentrations similar to and (c) catabolism. The activation step in the biosyn- 3 ␤ those produced by the microorganism, or by inocu- thesis of growth-promotive GAs is 3 -hydroxylation, lation with different Azospirillum spp. strains, can i.e. conversion of the 3-deoxy GA20 into the bioactive promote growth of roots in corn (Zea mays) seedlings GA1 (Kobayashi et al., 1994). Conjugation of GAs is (Fulchieri et al., 1990). It is interesting that inocula- tion with A. lipoferum promoted the appearance of 1 This research was suppported by the Consejo Nacional de free forms of GA3 in inoculated plant roots, whereas Investigaciones Cientı´ficas y Te´cnicas (CONICET grant no. PIP putative GA conjugates predominated in controls 4393 to R.B.), by the Secretarı´a de Ciencia y Te´cnica Universidad (Fulchieri et al., 1993). The latter results, however, Nacional de Rı´o Cuarto (grant to R.B.), and by the Consejo de did not establish whether the higher content of GA Investigaciones Cientı´ficas y Tecnolo´gicas de la Provincia de Co´r- 3 doba (CONICOR grant no. PID 3903 to R.B.). F.C. is the recipient found in the inoculated roots was due to de novo of a CONICET scholarship. production, hydrolysis by the microorganism per se, * Corresponding author; e-mail [email protected]; fax or by the plant under bacterial influence. Regarding 54–358–4676230. this issue, Piccoli et al. (1997) demonstrated that A. Plant Physiology, April 2001, Vol. 125, pp. 2053–2058, www.plantphysiol.org © 2001 American Society of Plant Physiologists 2053 Cassa´n et al. Ϯ Ͻ Table I. Length of second leaf sheath (in mm, p 0.05 confidence limits) of rice dy seedlings treated with GA A20 glucosyl conjugates and inoculated with Azospirillum spp. Treatments Noninoculated A. lipoferum Strain USA 5b A. brasilense Strain Cd 2 ␮ Ϫ1 [17,17- H2]GA20-G ( g plant ) 10Ϫ1 12.02 Ϯ 0.63 18.20 Ϯ 1.46 15.60 Ϯ 0.48 10Ϫ2 11.10 Ϯ 0.89 13.30 Ϯ 0.47 10.80 Ϯ 0.40 10Ϫ3 10.40 Ϯ 0.48 12.00 Ϯ 1.09 10.60 Ϯ 0.80 2 ␮ Ϫ1 [17,17- H2]GA20-GE ( g plant ) 10Ϫ1 11.80 Ϯ 0.40 17.20 Ϯ 1.46 17.40 Ϯ 0.80 10Ϫ2 11.60 Ϯ 0.80 13.40 Ϯ 0.48 13.40 Ϯ 1.01 10Ϫ3 11.00 Ϯ 0.63 11.75 Ϯ 0.82 11.00 Ϯ 0.89 Ethanol 95% (v/v) ϩ buffer 9.33 Ϯ 0.74 10.60 Ϯ 0.80 10.40 Ϯ 0.48 lipoferum grown in chemically defined medium has could also slightly reverse dwarfism, relative to eth- 2 the capacity to hydrolyze in vitro [17,17- H2]GA20 anol control treatments (Table I). Thus, it seems likely 2 glucosyl ester (GA20-GE) and [17,17- H2]GA20 glu- that the plant has some intrinsic capacity to hydro- cosyl ether (GA20-G). lyze GA-glucosyl conjugates. The difference in In a number of rice (Oryza sativa) cultivars the growth for inoculated versus noninoculated seed- dwarf phenotype is expressed in several single-gene lings can best be explained as hydrolytic plus meta- mutants. One mutant, dx, blocks at the level of kau- bolic activity of the bacteria on the conjugate. Al- rene oxidation; a second dwarf, dy, blocks the 3␤- though dwarfism reversal was observed in hydroxylation step (Takahashi and Kobayashi, 1991; treatments with each addition of GA-glucosyl conju- Kobayashi et al., 1994). gates, or with independent inoculation, the greatest We report herein the bacterial hydrolysis and me- growth increases were observed for those seedlings tabolism of GA conjugates in these two dwarf mu- that received the conjugated hormones as well as the tants of rice by endophytic Azospirillum spp. microorganism. There were no significant differences 2 between seedlings treated with [17,17- H2]GA20-G or 2 RESULTS [17,17- H2]GA20-GE. Thus, no particular Azospirillum spp. specificity for substrate was found. Reversal of the Dwarf (dy) Phenotype in Rice The responses of the dy rice mutant seedlings 2 2 Reversal of the Dwarf (dx) Phenotype in Rice treated with [17,17- H2]GA20-G and [17,17- H2]GA20- GE at several concentrations and/or inoculated with The responses of the rice dx mutant treated with 2 A. brasilense strain Cd and A. lipoferum strain USA 5b decreasing concentrations of [17,17- H2]GA20-G and 2 are shown in Table I. Both strains were effective in [17,17- H2]GA20-GE and inoculated with both A. promoting growth of seedlings and reversing dwarf- brasilense strain Cd and A. lipoferum strain USA 5b are ism when the two types of GA20-glucosyl conjugates shown in Table II. Internode length of inoculated were added. The promotive effects were similar for seedlings was significantly longer relative to nonin- each of the two forms of GA20-glucosyl conjugates. oculated treatments for the higher concentration of 2 2 Inoculated control plants (but without GA20 conju- [17,17- H2]GA20-G and [17,17- H2]GA20-GE. A. gate application) also showed dwarfism reversal, brasilense strain Cd and A. lipoferum strain USA 5b having a significantly greater growth than the were effective in promoting growth of seedlings and ethanol-treated controls. Treatments with deuterated reversing dwarfism when deuterated glucosyl conju- GA glucosyl conjugates alone (no Azospirillum spp.) gates were added, relative to noninoculated treat- Ϯ Ͻ Table II. Length of second leaf sheath (in mm, p 0.05 confidence limits) of rice dx seedlings treated with GA A20 glucosyl conjugates and inoculated with Azospirillum spp. Treatments Noninoculated A. lipoferum Strain USA 5b A. brasilense Strain Cd 2 ␮ Ϫ1 [17,17- H2]GA20-G ( g plant ) 10Ϫ1 17.60 Ϯ 1.85 21.80 Ϯ 1.32 23.60 Ϯ 1.35 10Ϫ2 12.60 Ϯ 0.48 14.20 Ϯ 0.97 13.40 Ϯ 0.80 10Ϫ3 10.00 Ϯ 0.63 10.40 Ϯ 0.48 12.00 Ϯ 0.63 2 ␮ Ϫ1 [17,17- H2]GA20-GE ( g plant ) 10Ϫ1 21.50 Ϯ 0.50 29.80 Ϯ 1.32 30.80 Ϯ 1.46 10Ϫ2 15.60 Ϯ 0.48 17.40 Ϯ 0.48 17.00 Ϯ 0.89 10Ϫ3 10.40 Ϯ 1.01 11.20 Ϯ 0.74 11.40 Ϯ 1.35 Ethanol 95% (v/v) ϩ buffer 12.30 Ϯ 0.50 13.60 Ϯ 1.01 13.40 Ϯ 0.74 2054 Plant Physiol.
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