Responses of Sorghum and Pennisetum Species to the N2-Fixing Bacterium Azospirillum brasilense

Three field inoculation experiments, two in Florida and one in New Mexico, were conducted with Azospirillum brasilense Cd. Each of the Florida experiments evaluated two crop species. One species in each of the Florida experiments responded to inoculation with a significant dry matter yield increases of 11 to 24% and nitrogen yield increases of 9 to 39%. No inoculation response was noted in the New Mexico experiment. The responding species were Sorghum bicolor (L.) Moench (sorghum) and the interspecific hybrid between Pennisetum americanum (L.) K. Schum. (pearl millet) and P. purpureum Schumach. (napiergrass). Nonresponding species were pearl millet (Florida) and Sorghum sudanense (Piper) Staph. (New Mexico). Acetylene reduction activity of inoculated plots in Florida was low, showing no increase over the natural uninoculated background rates and, in one case, was negatively correlated with yield. Acetylene reduction activity was not measured in New Mexico. In Florida, A. brasilense populations were found to decline from 5 × 10³ to 5 × 10² bacteria g of soil⁻¹ in about 3 weeks (quadratic regressions). Continued decline to less than 10² by week 5 indicated that the inoculated bacteria did not become established in the soil in high numbers. The A. brasilense population declined at about the same rate in the New Mexico experiment. The erractic inoculation responses in these experiments are similar to those observed in earlier work at the University of Florida. The lack of acetylene reduction activity response to inoculation and the rapid population decline of the inoculated bacteria suggest that N₂ fixation is not the major mechanism causing yield responses after inoculation.     

Association between N2-fixing bacteria and pearl millet plants: Responses,mechanisms and persistence

Responses to inoculation with N₂-fixing bacteria were studied in relation to genotypic differences in pearl millet, effect of nitrogen levels, and FYM additions in India. In some experiments, inoculation increased mean grain yield up to 33% over the uninoculated control, whereas in the remaining 11 experiments there was no significant increase. Increased grain yields, >10% over the uninoculated controls were observed in 46% of the experiments withAzospirillum lipoferum (18.7% average increase) and withAzotobacter chroococcum (13.6% average increase). Yield increases were nil or reduced in three experiments withAzos. lipoferum and four experiments withAztb. chroococcum. In two experiments continued inoculation for two or three years resulted in increased grain, plant biomass yield, and N uptake. Interactions of bacterial cultures with cultivars or years were not observed. The counts of the inoculated strains increased two to three-fold when inoculation was continued for three years. Repeated inoculations increased the mean cumulative N uptake from season 1 to season 3 by 19 kg ha^–1. Repeated inoculations withAztb. chroococcum andAzos. lipoferum increased mean grain yield of a succeeding crop by 14.4% and 9.8%, respectively, over the uninoculated control. Inoculation increased the efficiency of N-assimilation by pearl millet. Marginal increase in nitrogenase activity, associated with the inoculated plants was observed during later stages of plant growth. Increased leaf nitrate reductase activity (NRA) was observed after inoculation with these bacteria. The responses to inoculation are mainly attributable to increased plant N assimilation which could be the effect of growth promoting substances secreated by the bacteria; and thus the contribution from BNF may be small.CRISAT, journal article 732.     

Plant Growth Substances Produced by Azospirillum brasilense and Their Effect on the Growth of Pearl Millet (Pennisetum americanum L.)

Azospirillum brasilense, a nitrogen-fixing bacterium found in the rhizosphere of various grass species, was investigated to establish the effect on plant growth of growth substances produced by the bacteria. Thin-layer chromatography, high-pressure liquid chromatography, and bioassay were used to separate and identify plant growth substances produced by the bacteria in liquid culture. Indole acetic acid and indole lactic acid were produced by A. brasilense from tryptophan. Indole acetic acid production increased with increasing tryptophan concentration from 1 to 100 μg/ml. Indole acetic acid concentration also increased with the age of the culture until bacteria reached the stationary phase. Shaking favored the production of indole acetic acid, especially in a medium containing nitrogen. A small but biologically significant amount of gibberellin was detected in the culture medium. Also at least three cytokinin-like substances, equivalent to about 0.001 μg of kinetin per ml, were present. The morphology of pearl millet roots changed when plants in solution culture were inoculated. The number of lateral roots was increased, and all lateral roots were densely covered with root hairs. Experiments with pure plant hormones showed that gibberellin causes increased production of lateral roots. Cytokinin stimulated root hair formation, but reduced lateral root production and elongation of the main root. Combinations of indole acetic acid, gibberellin, and kinetin produced changes in root morphology of pearl millet similar to those produced by inoculation with A. brasilense.     

The influence of shading on associative N2 fixation

Summary The effect of reduced solar radiation on associative N₂-fixation and plant parameters was studied in three field experiments (1978–80). Gahi-3 pearl millet (Pennisetum americanum (L.) K. Monch.) field plots were shaded with saran shade cloth that reduced solar radiation by 50% and 75%. Acetylene reduction activity (ARA) was reduced by shading in one of the three experiments. The two non-responding experiments were conducted on a wall-drained, low-activity site (ARA means ranging 17–68 n moles ethylene core^–1 h^–1), the responding experiment was conducted on a poorly drained, high-ARA site.Shading affected the plants drastically, reducing fresh weight and dry matter yields up to 46% (50% shade) and 57% (75% shade). Shading also reduced dry matter percentage from 19.6 (no shade) to 15.3 (75% shade) and increased nitrogen content from 0.6% (no shade) to 1.53% (75% shading). However, shading did not affect protein yield. Inoculation withAzospirillum brasilense had no measurable effect on yield or acetylene reduction in the first two experiments.In the third experiment, shading reduced mean ARA of inoculated plots over 100% but had no significant effect on control plots. Inoculation significantly increased ARA in the nonshaded plots but not in shaded plots. Acetylene reduction activity was high, with means ranging between 208 and 465 n moles ethylene evolved core^–1 h^–1. Soil moisture and millet growth stage also affected acetylene reduction activity.     

Effect of combined inoculation ofAzospirillum brasilense and vesicular-arbuscular mycorrhiza on pearl millet (Pennisetum americanum)

Summary Growth and phosphorus uptake of pearl millet (Pennisetum americanum) on an unsterile, phosphorus-deficient soil was improved by the seed inoculation withAzospirillum brasilense or soil inoculation with the vesicular-arbuscular mycorrhizal fungi (Acaulospora,Gigaspora margarita, Glomus fasciculatum). These microorganisms acted synergistically when added simultaneously and the response was significant withAzospirillum brasilense + Gigaspora margarita andAzospirillum brasilense + Glomus fasciculatum combinations over uninoculated control as far as the dry matter content of shoots, root biomass and phosphorus uptake of the millet was concerned.     

N(2) Fixation by Azospirillum brasilense and Its Incorporation into Host Setaria italica

Growth and nitrogen fixation were followed during the life cycle of Setaria italica (foxtail millet) inoculated with Azospirillum brasilense in controlled-environment growth chambers. The plants were fertilized at seeding with a limiting amount of combined nitrogen and maintained with an N-free mineral solution. During maturation of the plants, substantial nitrogenase activity, measured by acetylene reduction, developed in the rhizosphere, with total fixation estimated to be equivalent to 20% of the N in the inoculated plants. The peak of this activity coincided with depletion of soluble nitrogen from the system, which in turn was reflected by a sharp decrease in the nitrate reductase activity of the leaves. A. brasilense was found in association with the root populations at 8 x 10 cells per gram of dry weight. An increase in shoot growth occurred at this time, but no significant increase in total plant nitrogen could be demonstrated. N(2) enrichment experiments confirmed that fixation was occurring, but only about 5% of the nitrogen fixed by A. brasilense was incorporated into the plants within 3 weeks. There was thus no evidence of direct bacterium-to-plant transport of fixed nitrogen, but rather a slow transfer suggesting the gradual death of bacteria and subsequent mineralization of their nitrogen, at least under growth-room conditions.     

Hypersensitive response, cell death and histochemical localisation of hydrogen peroxide in host and non-host seedlings infected with the downy mildew pathogen Sclerospora graminicola

Hypersensitive response, cell death and release of hydrogen peroxide as measures of host and non‐host defense mechanisms upon inoculation with the downy mildew pathogen Sclerospora graminicola were studied histochemically at the light microscopy level. The materials consisted of coleoptile tissues of the highly susceptible (cv. HB3), highly resistant (cv. IP18293) and induced resistant pearl millet host seedlings and non‐host sorghum (cv. SGMN10/8) and cotyledon of french bean (cv. S9). Resistance up to 80% protection against the downy mildew pathogen was induced in the highly susceptible HB3 cultivar of pearl millet by treating the seeds with 2% aqueous leaf extract of Datura metel for 3 h. Time course study with the pathogen inoculated highly resistant pearl millet cultivar revealed the appearance of hypersensitive response in 20% of seedlings as necrotic spots as early as 2 h after inoculation. In contrast, a similar reaction was observed in the highly susceptible pearl millet cultivar only 8 h after inoculation with the pathogen. In induced resistant seedlings, appearance of hypersensitive response was recorded 4 h after inoculation. Delayed hypersensitive response was observed in both the non‐host species at 10 h after inoculation. Hypersensitive response in the seedlings of the highly resistant pearl millet cultivar 24 h after inoculation showed 100% hypersensitive response, which was not observed in susceptible and non‐host species, although the induced resistant seedlings showed 90% hypersensitive response after that period of time. Cell death in the tissues of the test seedlings was also observed to change with time. Statistical analysis revealed that the tissues of highly resistant pearl millet seedlings required 2.9 h to attain 50% cell death. Tissues of induced resistant and highly susceptible pearl millet seedlings required 4.65 and 6.50 h respectively. In non‐hosts, 50% cell death was not recorded. Quantification of hydrogen peroxide in the tissue periplasmic spaces of the test seedlings revealed 2.94 h as the time required for 50% hydrogen peroxide accumulation in the tissues of highly resistant pearl millet seedlings. Tissues of induced resistant and highly susceptible pearl millet seedlings needed 3.76 and 5.5 h respectively. Fifty percent hydrogen peroxide localisation in non‐hosts could not be recorded. These results suggested the involvement of hydrogen peroxide, cell death and hypersensitive response in pearl millet host defense against S. graminicola.     

Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants

Bacteria of the genus Azospirillum increase the grain yield of several grass crops. In this work the effect of inoculating maize plants with genetically engineered Azospirillum brasilense for trehalose biosynthesis was determined. Transformed bacteria with a plasmid harboring a trehalose biosynthesis gene-fusion from Saccharomyces cerevisiae were able to grow up to 0.5 M NaCl and to accumulate trehalose, whereas wild-type A. brasilense did not tolerate osmotic stress or accumulate significant levels of the disaccharide. Moreover, 85% of maize plants inoculated with transformed A. brasilense survived drought stress, in contrast with only 55% of plants inoculated with the wild-type strain. A 73% increase in biomass of maize plants inoculated with transformed A. brasilense compared with inoculation with the wild-type strain was found. In addition, there was a significant increase of leaf and root length in maize plants inoculated with transformed A. brasilense . Therefore, inoculation of maize plants with A. brasilense containing higher levels of trehalose confers drought tolerance and a significant increase in leaf and root biomass. This work opens the possibility that A. brasilense modified with a chimeric trehalose biosynthetic gene from yeast could increase the biomass, grain yield and stress tolerance in other relevant crops.     

Nitrate concentration and nitrate reductase activity in the leaves of three legumes and three cereals*

Nitrate concentration and nitrate reductase activity (NRA) were studied in the leaves of soybean (Glycine max), groundnut (Arachis hypogaea and cowpea (Vigna unguiculata) and sorghum (Sorghum bicolor), pearl millet (Pennisetum americanum) and maize (Zea mays) at three nitrogen fertiliser levels in two field experiments. Higher nitrate concentrations were detected in the leaves of groundnut, cowpea and pearl millet than in sorghum and maize. Nitrate content in the leaves and leaf NRA were not related across crop species, nor was a generalised pattern of leaf NRA and leaf nitrate observed within legumes or within cereals. Nitrogen application resulted in higher nitrate availability in the leaves, with varied leaf NRA.     

Differential responses of growth and nitrogen uptake to organic nitrogen in four gramineous crops

The capability to utilize different forms of nitrogen (N) by sorghum (Sorghum bicolor), rice (Oryza sativa), maize (Zea mays), and pearl millet (Pennisetum glaucum) was determined in pot experiments. Seedlings were grown for 21 d without N, or with 500 mg N kg(-1) soil applied as ammonium nitrate, rice bran or a mixture of rice bran and straw. No treatment-dependent changes of root length, surface area, and fractal dimension were observed. Shoot growth and N uptake in maize and pearl millet correlated with the inorganic N (ammonium and nitrate) concentration in the soil, suggesting that these species depend upon inorganic N uptake. On the other hand, shoot growth and N uptake patterns in sorghum and rice indicated that these two species could compensate low inorganic N levels in the organic material treatments by taking up organic N (proteins). Analysis of N uptake rates in solution culture experiments confirmed that sorghum and rice roots have higher capabilities to absorb protein N than maize and pearl millet.     

Possible role of alternative respiration in temperature rise of water stressed plants

Role of alternative respiration, a thermogenic pathway, was evaluated in temperature rise of water stressed plants. Transpiration rate, plant temperature and respiratory dynamics were monitored in field grown irrigated and unirrigated sorghum(Sorghum vulgare Pers.) hybrid CSH 6 and pearl millet(Pennirelum typhoider (Burm. f.) Stapt and Hubbard) var. J 104 for 22 days. Transpiration rate of irrigated plants was always higher than the unirrigated plants. But the plant temperature and the alternative respiration activity of irrigated plants was always lower than unirrigated plants. The reduction in transpiration rate of unirrigated pearl millet was more as compared to unirrigated sorghum. Nonetheless, alternative respiration activity was higher in unirrigated sorghum as compared to unirrigated pearl millet. Temperature of unirrigated sorghum plants increased by 10.4°C during 22 days and it was 8.0°C higher than irrigated sorghum at day 22. Stressed pearl millet showed an increase of 3.9°C during 22 days and it was 2.9°C higher than the irrigated pearl millet at day 22. It is suggested that the heat released because of the alternative respiration activity also contributes towards temperature rise of water stressed plants.     

Survival of Azospirillum brasilense in the Bulk Soil and Rhizosphere of 23 Soil Types

The survival of Azospirillum brasilense Cd and Sp-245 in the rhizosphere of wheat and tomato plants and in 23 types of plant-free sterilized soils obtained from a wide range of environments in Israel and Mexico was evaluated. Large numbers of A. brasilense cells were detected in all the rhizospheres tested, regardless of soil type, bacterial strain, the origin of the soil, or the amount of rainfall each soil type received prior to sampling. Survival of A. brasilense in soils without plants differed from that in the rhizosphere and was mainly related to the geographical origin of the soil. In Israeli soils from arid, semiarid, or mountain regions, viability of A. brasilense rapidly declined or populations completely disappeared below detectable levels within 35 days after inoculation. In contrast, populations in the arid soils of Baja California Sur, Mexico, remained stable or even increased during the 45-day period after inoculation. In soils from Central Mexico, viability slowly decreased with time. In all soils, percentages of clay, nitrogen, organic matter, and water-holding capacity were positively correlated with bacterial viability. High percentages of CaCO(inf3) and fine or rough sand had a highly negative effect on viability. The percentage of silt, pH, the percentage of phosphorus or potassium, electrical conductivity, and C/N ratio had no apparent effect on bacterial viability in the soil. Fifteen days after removal of inoculated plants, the remaining bacterial population in the three soil types tested began to decline sharply, reaching undetectable levels 90 days after inoculation. After plant removal, percolating the soils with water almost eliminated the A. brasilense population. Viability of A. brasilense in two artificial soils containing the same major soil components as the natural soils from Israel did was almost identical to that in the natural soils. We conclude that A. brasilense is a rhizosphere colonizer which survives poorly in most soils for prolonged periods of time; that outside the rhizosphere, seven abiotic parameters control the survival of this bacterium in the soil; and that disturbance of the soil (percolation with water or plant removal) directly and rapidly affects the population levels.     

Comparative analysis of activities of vital defence enzymes during induction of resistance in pearl millet against downy mildew

Pearl millet [Pennisetum glaucum (L.) R. Br.] has the seventh largest annual production in the world giving it significant economic importance. Although generally well adapted to the growing conditions in arid and semi-arid regions, major constraints to yields are susceptibility to downy mildew disease caused by the oomycete Sclerospora graminicola (Sacc.) Schroet. Induction of resistance against downy mildew disease of pearl millet has been well established using various biotic and abiotic inducers. The present study demonstrated the comparative analysis of the involvement of the important defence enzymes like β-1,3-Glucanase, chitinase, phenylalanine ammonia-lyase (PAL), peroxidase (POX), polyphenol oxidase (PPO) and lipoxygenase (LOX) during induced systemic resistance (ISR) mediated by inducers like Benzo(1,2,3)-thiadiazole-7-carbothionic acid-S-methyl ester (BTH), Beta amino butyric acid (BABA), Chitosan and Cerebroside against pearl millet downy mildew disease. Native-PAGE showed six POX isozymes in all categories of uninoculated pearl millet seedlings and maximum intensity of bands was noticed in resistant seedlings. After inoculation in Cerebroside-treated seedlings, there were seven isoforms, POX-4 was not present in any other seedlings. Native-PAGE analysis showed the presence of five PPO isozymes in all categories of uninoculated pearl millet seedlings and after inoculation seven isoforms of PPO-7 were noticed, and the intensity of banding was more in resistant and Cerebroside-treated seedlings. The isoforms PPO-3 were present as an extra band after inoculation in all seedlings. Isoform PPO-7, though found in all seedlings, was very prominent in Chitosan- and Cerebroside-treated seedlings. β-1,3-Glucanase Native-PAGE analysis showed the presence of only one isozyme in all categories of uninoculated/inoculated pearl millet seedlings. Glu-1 isozyme was very prominent in all seedlings including resistant and susceptible seedlings. Among the induced resistant seedlings, highest intensity was observed in Cerebroside-treated seedlings. Native-PAGE analysis showed the presence of three LOX isozymes in all categories of uninoculated pearl millet seedlings, and the intensity of banding pattern was very low in BTH-treated seedlings. LOX-1 and LOX-2 were very prominent in resistant, Chitosan- and Cerebroside-treated seedlings. Upon inoculation, one extra band, LOX-3, was exclusively noticed in Cerebroside-treated seedlings. In inoculated seedlings, LOX-1, LOX-2 and LOX-4 were very prominent in Chitosan Cerebroside-treated seedlings compared to other seedlings.     

Effect of inoculation of Zea mays with Azospirillum brasilense strains under temperate conditions

Seven strains of Azospirillum brasilense were compared for their effect on the growth of Zea mays grown under temperate conditions in sand--vermiculite pot cultures. Inoculation with all seven strains tested, including Fix(-) mutant strains, increased dry weight and total nitrogen content of shoots, but nitrogen concentrations were unaffected. Low and variable rates of acetylene reduction activity were observed from excised roots of inoculated plants without preincubation. Estimates of N2-fixing A. brasilense associated with inoculated roots showed differences between strains in establishing themselves in the rhizosphere and endorhizosphere. In some strains enrichment in the endorhizosphere of roots occurred following inoculation, but the relative numbers and location of the strains did not appear to affect the yield response.     

Improvement in bioavailability of tricalcium phosphate to Cymbopogon martinii var. motia by rhizobacteria, AMF and Azospirillum inoculation

The interactive effects of phosphate solubilizing bacteria, N2 fixing bacteria and arbuscular mycorrhizal fungi (AMF) were studied in a low phosphate alkaline soil amended with tricalcium insoluble source of inorganic phosphate on the growth of an aromatic grass palmarosa (Cymbopogon martinii). The microbial inocula consisted of the AM fungus Glomus aggregatum, phosphate solubilizing rhizobacteria Bacillus polymyxa and N2 fixing bacteria Azospirillum brasilense. These rhizobacteria behaved as "mycorrhiza helper" and enhanced root colonization by G. aggregatum in presence of tricalcium phosphate at the rate of 200 mg kg(-1) soil (P1 level). Dual inoculation of G. aggregatum and B. polymyxa yielded 21.5 g plant dry weight (biomass), while it was 21.7 g in B. polymyxa and A. brasilense inoculated plants as compared to 14.9 g of control at the same level. Phosphate content was maximum (0.167%) in the combined treatment of G. aggregatum, B. polymyxa and A. brasilense at P1 level, however acid phosphatase activity was recorded to be 4.75 pmol mg(-1) min(-1) in G. aggregatum, B. polymyxa and A. brasilense treatment at P0 level. This study indicates that all microbes inoculated together help in the uptake of tricalcium phosphate which is otherwise not used by the plants and their addition at 200 mg kg(-1) of soil gave higher productivity to palmarosa plants.     

Activity of two catabolic enzymes of the phosphogluconate pathway in mesquite roots inoculated with Azospirillum brasilense Cd.

The mesquite amargo (Prosopis articulate), one of the main nurse trees of the Sonoran Desert in Mexico, is responsible for major, natural re-vegetation processes. It exudes gluconic acid in root exudates, a favorite carbon source for the plant growth-promoting bacterium Azospirillum brasilense. Two enzymes, gluconokinase (EC 2.7.1.12) and 6-phosphogluconate dehydrogenase (EC 1.1.1.44), participating in the phosphogluconate pathway, are active in the bacteria. Bacterial 6-phosphogluconate dehydrogenase is a constitutive enzyme, while gluconokinase is induced upon exposure to gluconic acid. Both enzymes are active in young, non-inoculated mesquite seedlings growing under hydroponic conditions. When A. brasilense Cd bacteria are inoculated on the root system, the roots exhibit much higher activity of gluconokinase, but not 6-phosphogluconate dehydrogenase. Mesquite roots exhibit high levels of root colonization by the inoculating bacteria. At the same time, and also for plants growing under sand culture conditions, the seedlings grew taller, greener, had longer leaves, and were heavier.     

Effect of Four Sowing Date Environments on Growth, Development and Yield Potentials of 15 Pearl Millet Cultivars (Pennisetum americanum L Leeke) During Autumn-Winter Seasons in Marin, N.L., Mexico

A study has been undertaken on the growth, development, andyield potentials of 15 pearl millet cultivars showing a largegenetic variability in growth parameters in different sowingenvironments Sowing date had a significant effect on growthstages (GS1, GS2, GS3), thermal units accumulated in respectivegrowth stages, days to flowering, and yield components of thepearl millet cultivars Significant genotype x sowing date interactionswere also observed for the majority of the variables mentioned. A decline in both temperature and length of photopenod oversuccessive sowing dates from July to September had a drasticeffect on phenology and yield potentials of the pearl milletcultivars. Higher grain yield in the July sowing experiment, compared tothose for other sowing dates, could be related to a longer photopenod(> 13 h), higher temperatures, and a significant differencebetween day and night temperatures. Key words: Environment, growth, yield potentials, thermal units, pearl millet     

The Possible Involvement of Lipoxygenase in Downy Mildew Resistance in Pearl Millet

The downy mildew disease, incited by Sclerospora graminicola,is a major biotic constraint for pearl millet production inthe semi-arid tropics. Sources of resistance to this diseasehave been identified. However, the mechanism of host resistancestill remains obscure. The enzyme lipoxygenase (LOX) is knownto play a role in disease resistance in many host-pathosystems.In the present study, LOX activity was tested in seeds of differentgenotypes of pearl millet with different susceptibility to downymildew. The LOX assay of the seeds indicated a good correlationbetween enzyme activity and their downy mildew reaction in thefield. Maximum activity was recorded in seeds of highly resistantgenotypes and minimum activity was found in the highly susceptiblegenotypes. Seeds obtained from plants recovered from the downymildew disease had more LOX activity than that of the originalparent seeds. Thus, in seeds, the LOX activity can be used asa biochemical marker for screening different genotypes of pearlmillet for downy mildew. The study, carried out in the susceptiblegenotype of pearl millet seedlings, showed that LOX activitydecreased after inoculating with S. graminicola zoospores whencompared with uninoculated controls. However, a significantincrease in the enzyme activity was observed on the second andthird days after inoculation in resistant seedlings. The possiblerole of LOX in conferring resistance to downy mildew infectionof pearl millet is discussed. Key words: Lipoxygenase, pearl millet, downy mildew     

巴西固氮螺菌Yu62由水稻和烟草根部向茎、叶的迁移运动(英文)

巴西固氮螺菌(Azospirillum brasilence)是重要的植物促生内生菌之一。用gfp基因标记固氮螺菌后接种无菌的水稻和烟草幼苗的根部,限菌培养一定时间后,用共聚焦激光显微镜观察,结果表明:除了根内部有发荧光的螺菌定殖外,螺菌还分布在茎、叶的表皮细胞,皮层细胞和维管系统组织的细胞和细胞间隙。从根、茎、叶器官分离固氮螺菌,都存在有较高的螺菌群体密度。这一结果证明螺菌在植物内存在着从根部向茎、叶顶端的迁移现象。这一发现为研究巴西固氮螺菌在宿主植物体内的迁移运动的机制、与植物细胞间的分子相互作用及其对植物的促生作用奠定了生态学和细胞形态学的基础,也为实际应用提供了进一步的科学依据,具有重要的科学和实践意义。