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Article

Screening Digitaria eriantha cv. Suvernola Endophytic Bacteria for Maize Growth Promotion

by
Michelle J. G. Alves
1,
Johny Jesus Mendonça
1,2,
Gisely Moreira Vitalino
1,
José Paula Oliveira
3,
Erix Xavier Carvalho
3,
Felipe José Cury Fracetto
1,
Giselle Gomes Monteiro Fracetto
1 and
Mario Andrade Lira Junior
1,*
1
Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife 52171-900, Brazil
2
Programa de Pós-Graduação em Ciência do Solo, Universidade Federal do Rio Grande do Sul, Porto Alegre 91501-970, Brazil
3
Instituto Agronômico de Pernambuco, Recife 50171-000, Brazil
*
Author to whom correspondence should be addressed.
Plants 2023, 12(14), 2589; https://doi.org/10.3390/plants12142589
Submission received: 30 May 2023 / Revised: 5 July 2023 / Accepted: 7 July 2023 / Published: 8 July 2023
(This article belongs to the Special Issue Plant–Microbe Interactions for Sustainable Agriculture)
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Abstract

:
The search for sustainable agriculture has increased interest in using endophytic bacteria to reduce fertilizer use and increase stress resilience. Stress-adapted plants are a potential source of these bacteria. Some species of these plants have not yet been evaluated for this, such as pangolão grass, from which we considered endophytic bacteria as potential plant growth promoters. Bacteria from the root, colm, leaves, and rhizospheric soil were isolated, and 132 strains were evaluated for their in vitro biological nitrogen fixation, IAA and siderophores production, and phosphate solubilization. Each mechanism was also assessed under low N availability, water stress, and low-solubility Fe and P sources in maize greenhouse experiments. All strains synthesized IAA; 63 grew on N-free media, 114 synthesized siderophores, and 46 solubilized P, while 19 presented all four mechanisms. Overall, these strains had better performance than commercial inoculant in all experiments. Still, in vitro responses were not good predictors of in vivo effects, which indicates that the former should not be used for strain selection, since this could lead to not testing strains with good plant growth promotion potential. Their heterologous growth promotion in maize reinforces the potential of stress-adapted plant species as potential sources of strains for inoculants.

1. Introduction

Population growth demands increased food production, while current and forecasted environmental conditions require a significant decrease in agriculture’s ecological footprint. This has led to the increasing use of plant-growth-promoting bacteria (PGPB), since these can reduce fertilizer use and increase crops’ resilience to environmental stresses [1]. These are usually endophytic or rhizospheric bacteria that do not provoke any harm to the plant and may, under some conditions, promote their growth or reduce the effects of environmental stresses [2].
Endophytic bacteria may increase plant growth and adaptation to environmental stress [3]. This plant growth promotion is variously credited to several mechanisms, such as biological nitrogen fixation, synthesis and release of phytohormones such as IAA, phytopathogen control through synthesis and release of siderophores, or phosphate solubilization, several of which are frequently evaluated under in vitro conditions [4,5,6].
These mechanisms are widely distributed in several bacterial genera, such as Acetobacter, Aerobacter, Aeromonas, Agrobacterium, Azospirillum, Bacillus, Burkholderia, Chryseomonas, Curtobacterium, Enterobacter, Erwinia, Flavimonas, Gluconacetobacter, Herbaspirillum, Klebsiella, Pseudomonas, Rhizobium, and Sphingomonas, which have been isolated as endophytic from a broad spectrum of plant species, such as maize, wheat, rice, sugarcane, sorghum, and signal grass [7,8,9,10,11,12].
On the other hand, several plant species well adapted to stressful environments, such as pangolão grass (Digitaria eriantha cv. Survenola), have not been well studied until now, even though we have found it to harbor a very diverse bacterial endophyte population [13], since the literature contains several examples of plants from these environments being effective sources of plant-growth-promoting bacteria [14,15,16]. At the same time, it is also known that bacteria isolated from one species may be highly effective on another; for example, as happens with the commercial inoculants based on Azospirillum brasilense in Brazil [17]. Other example is the use of bacteria isolated from Stipa tenacissima L. and used to reduce salt stress on tomato [16], from Opuntia ficus-indica increasing wheat growth under drought [18], from garlic on common beans growth [19], or from Suaeda nudiflora on Amaranthus viridis under salt stress [3].
We aim, thus, to evaluate this diversity as a source of plant-growth-promoter bacteria both in vitro and for maize plants.

2. Results

2.1. Plant-Growth-Promoting Characteristics of Endophytic Isolates

The most frequent in vitro growth-promoting mechanism was IAA production, which occurred in all strains ranging from ca. 4 to ca. 212 μg mL−1, followed by siderophores (86%, ranging from 1 to 83%), BFN (48%), and phosphate solubilization (35%, with SI from 1 to 3) (Figure 1) (Table S1).

2.2. Binding of In Vitro Growth-Promoting Mechanisms

Grouping these characteristics led to eight groups with 100% similarity (Figure 2). Group I (GI) included two strains that grew without N and produced IAA, while GII also had two strains that, besides the above, also solubilized phosphate. GIII with four strains was like GII but did not grow in N-free media. In comparison, the 10 strains of GIV could only produce IAA, the 19 strains of GV presented all mechanisms, and the 40 strains of GVI had all but P solubilization. GVII is formed by 34 IAA- and siderophore-producing strains, and GVIII by 21 strains with all mechanisms bar growth in N-free media.

2.3. Efficiency of Growth-Promoting Bacteria in the Early Stage of Maize

Generally, the pangolão isolated strains yielded higher results than CI for at least two variables in the N-restricted experiment (Table 1). Although no strain led to significantly higher SDM than CI, several were significantly higher in RECI, indicating an overall higher growth promotion activity. However, all were significantly lower in RE + C than the +C treatment, indicating that the growth promotion could not fully overcome N deficiency effects.
Although no strain from Pangolão led to higher LA than CI, most other variables had at least two strains with higher results (Table 2). Most importantly, two strains had higher SDM and RECI, while several increased RDM, and four achieved higher RE + C than fully irrigated plants.
Although no strain significantly differed from CI for any of the variables on the low-Fe solubility experiment (Table S2), plants with strain 252 were significantly higher, and strain 5227 had a higher SDM. While no strain achieved higher SDM, SAN, or relative efficiencies than CI, several led to significantly higher PH, CD, LA, RDM, and SAP (Table 3). Some had non-significant higher RE + C than +C plants.

2.4. Binding of In Vitro and In Vivo Growth-Promoting Mechanisms

Most in vitro plant-growth-promoting characteristics were not significantly correlated to plant growth effect in maize (Table 4), and even those which were significant, such as SI and PH for the siderophore experiment (r = 0.25, p < 0.01), or between SI and SDM in the P solubilization experiment (r = 0.30, p < 0.01), had relatively low predictive values.
As a group, strains that did not grow in N-free media had lower leaf area in the N-deficient experiment and increased RDM in the low-solubility Fe one (Table 5). At the same time, those positive for this mechanism reduced SAN and SAP in the water-deficit experiment. While low or average IAA synthesis led to generally higher results in the water-deficit experiment, those with high IAA synthesis increased RDM in the low-solubility P experiment. Medium SI strains had generally higher RDM in the low-solubility P experiment, while this was found for the high SI strains in the low Fe solubility experiment. These results, coupled with the low and mostly non-significant correlations between in vitro and maize results, indicate that these in vitro methods are not good predictors of plant effects.

3. Discussion

This is the first evaluation of the plant-growth-promoting potential of Pangolão grass endophytic bacteria, which is particularly interesting since endophytic bacteria from plants from stressful environments such as this might help reduce environmental stress effects on crops [5,18]. Strains previously isolated from this plant species [13] included several genera known to harbor plant-growth-promoting strains. Indeed, all 132 strains tested under in vitro conditions here had at least one commonly held plant-growth-promoting trait.
These traits occurred in different proportions when other plant species were evaluated. For example, while 48% of the strains grew in N-free media, strains from other grasses grown in the Brazilian tropical semiarid included 66% diazotrophs [20], and signal grass root and rhizosphere bacteria had 58% diazotrophs [21].
IAA production, on the other hand, seems to be much more widely spread, since 100% of the strains were positive for this trait, as also happened with strains from cold-tolerant rice [22,23], and strains from plants under saline conditions also had 86% occurrence for this trait [24]. A similarly frequent feature seems to be siderophore production since we found 86% of siderophore-producing strains and signal grass had very similar results at 84% occurrence [25].
Most Pangolão-isolated strains had at least one of the commonly evaluated in vitro growth-promoting characteristics [26], while strains with more than one of these tended to have stronger plant-growth-promoting effects under environmental stress [8]. This may indicate that these bacteria are an important part of Pangolão adaptation mechanisms to the environmental stress typical of where it was collected. This is furthered by the presence of Pantoea, Enterobacter, Rhizobium, Pseudomonas, and Stenotrophomonas strains, which are frequently described as promoting plant growth for several species [14,27,28,29,30,31,32].
The high proportion of in vitro plant growth characteristics found here agree with the frequent consideration that plants adapted to stressful environments tend to have plant-growth-promoting endophytic bacteria [8,26,33]. Although we evaluated only the initial maize growth, several strains increased some of the plant variables found in plants receiving a CI with known effective strains for this crop under low N availability [17]. This is likely due to IAA effects on root growth, and thus on water and nitrogen absorption [2].
Interestingly, the strains with higher N accumulation in the low-water-availability experiment were all identified as Rhizobium, Paenibacillus, and Agrobacterium species, all of which are known as potentially diazotrophic [34,35], which may indicate some level of unmeasured biological nitrogen fixation.
On the other hand, the small effects of both low P and Fe solubility experiments might be due to the early stage on which we harvested the maize, as also observed for wheat [32]. Still, even under those limiting conditions, some strains induced higher growth than the CI.
A common occurrence in our experiments was bacteria with low values for a given in vitro mechanism achieving higher than CI values for a plant-growth promotion in the experiment designed to evaluate that trait. This is coupled with a generally low and non-significant correlation between in vitro and maize effects and might be due to most of the strains presenting more than one of the mechanisms (Figure 2), as also proposed in the literature and in the typical indication of using a mix of strains for inoculant production [36,37,38,39,40].

4. Materials and Methods

Plant sampling, bacterial sampling, isolation, DNA extraction, BOX-PCR grouping, and sampling were all described in Alves et al. [13]. In short, endophytic and rhizospheric bacteria from Pangolão grass from three Pernambuco state municipalities were isolated, through serial dilutions in sterile saline solution, in semi-solid, N-free, NFB media [41], while in one of the locations, JNFB and JMV media were also used [42,43]. Where growth was observed in the N-free media, bacteria were transferred to YMA media for phenotypical characterization [44], followed by DNA extraction and BOX-PCR fingerprinting. Representative strains of the BOX-PCR 90% similarity groups had their 16S rRNA sequenced. They were chosen for the in vitro evaluation of biological nitrogen fixation [41], IAA production [45], calcium phosphate solubilization [46], and siderophore production [47].
Each of these mechanisms was later evaluated in a separate greenhouse experiment with maize to evaluate specific environmental stresses, such as low available nitrogen, water deficit, and low-solubility P and Fe sources, respectively.
All experiments were conducted in 5 L plastic vessels filled with sterile sand: vermiculite 1:1 mixture, using maize cultivar BR-5026, also known as São José. This cultivar is recommended for low-resource agriculture in tropical semiarid regions and was developed as a multipurpose cultivar for forage production, immature corn, or for grain production. It has dented yellow cobs, 300 cm tall plants, a 120-day cycle, and a stable yield.
Seeds were surface-disinfested with 70% ethanol for 30 s, immersed in 2.5% sodium hypochlorite for 2 min, washed eight times with sterile distilled water, and inoculated with 1 mL per seed of 109 cells.mL−1 bacterial broth of the strain under evaluation, according to standard Brazilian recommendations for the commercial inoculation of corn [17]. All experiments were conducted on a randomized block design with three replicates.
As biological nitrogen fixation is not considered to support all plant growth for non-legumes [48], all plants in this experiment were supplied with 30% of the recommended N dose at seeding. Twenty strains were evaluated; seven were positive for N-free media growth, and the remainder did not grow in this media (Table 6). The control treatments for this experiment were non-inoculated plants inoculated with the commercial Azospirillum brasilense inoculant AzzoFix® (CI). This is a liquid inoculant for corn with strains Ab-V5 and Ab-V6 and 2.0 × 108 UFC·mL−1, as defined and authorized according to Brazilian legislation [17], and 100% N dose supply (equivalent to 20 kg N·ha−1) (+C) under a low N input recommendation for the tropical semi-arid condition in Pernambuco state [49].
IAA was evaluated under water deficit stress since this mechanism is supposed to increase root growth, maintained by keeping the plants at ca. 30% pot-water-holding capacity after complete seed germination. Twenty-four strains were selected representing the 0–5, 5–25, 25–50, 50–75, 75–95, and 95–100 percentiles for in vitro IAA production (Table 6), with the same control treatments as above, except for the positive control substituted for the use of 100% pot-water holding capacity (+C).
For the P solubilization capacity, tri-calcium phosphate was used as the sole P source, and 21 bacterial strains were selected to represent the 0–75, 75–95, and 95–100 percentiles for in vitro P solubilization, respecting the proportion of non-solubilizing bacteria effectively found similarly to the BNF experiment (Table 6). Control treatments were similar to the previous experiments, with the positive control being triple superphosphate as the phosphorus source (+C).
Siderophore was evaluated by replacing the Fe source in the nutrient solution with a low-solubility one. In this case, 24 strains were selected to represent the 0–5, 5–25, 25–50, 50–75, 75–95, and 95–100 percentiles for in vitro siderophore production (Table 6), and the control treatments were similar to the previous experiments, with the positive control being a high-solubility Fe source (+C).
For all experiments, harvest was 20 days after emergence, plant height (PH), colm diameter (CD), and leaf area (LA) were measured, and root (RDM) and shoot dry matter (SDM) was determined. Traditional wet methods determined N and P contents, and shoot accumulated N (SAN) and P (SAP) were calculated by the product of shoot dry matter and the appropriate content.
We also calculated the relative efficiencies of each treatment in relation to the non-inoculated control (REN), commercial inoculant (RECI), and each positive control (RE + C). In all cases, these were calculated according to this equation.
R E % = T r e a t m e n t   S h o o t   D r y   M a t t e r A v e r a g e   S h o o t   D r y   M a t t e r   o f   t h e   a p p r o p r i a t e   c o n t r o l × 100                        
The in vitro data were grouped at 100% similarity using the Jaccard dissimilarity index and UPGMA. Maize data were evaluated for homoscedastic and outliers. When needed, they were transformed by log10 and elimination of outliers before ANOVA and Dunnett’s test at 5% significance using the commercial inoculant as the control treatment. Later, only the inoculant treatments were evaluated, considering their grouping from the in vitro evaluations, as described for each experiment, and considering the variation within each group as a random effect. The Pearson linear correlation was evaluated for each experiment, considering the in vitro values and the plant variables.

5. Conclusions

Endophytic bacteria strains from pangolão grass increased initial plant growth for at least some variables of those provided by known effective Azospirillum strains under four different environmental stress conditions, likely due to this plant being adapted to stressful environments. Thus, its microbiome is an essential component of this adaptation.
The lack of substantial predictive value for the in vitro plant-growth-promotion characteristics, as seen by the low and generally non-significant correlations and the apparent disconnect between these and plant effects, indicates that the common practice of choosing strains for plant evaluation based on the in vitro evaluation might be flawed and needlessly reduce the genetic diversity in the plant evaluation.
Although the maize experiments were designed to evaluate specific environmental stresses purportedly linked to each in vitro plant-growth-promoting characteristic, the plant promotion is not directly related to individual mechanisms.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants12142589/s1, Table S1: In vitro growth promotion evaluation. BNF—growth in N-free media. IAA—IAA synthesis. SI—calcium phosphate solubilization index. Siderophore—siderophore synthesis; Table S2: Evaluation of strains associated with pangolan grass in terms of in vivo siderophore production and corn growth 20 days after germination.

Author Contributions

Conceptualization, M.J.G.A. and M.A.L.J.; Methodology, M.J.G.A., J.J.M., G.M.V., E.X.C. and M.A.L.J.; Investigation, M.J.G.A., J.J.M. and G.M.V.; Formal Analysis, M.J.G.A., E.X.C. and M.A.L.J.; Funding Acquisition, E.X.C., J.P.O. and M.A.L.J.; Supervision, E.X.C., J.P.O., F.J.C.F., G.G.M.F. and M.A.L.J.; Writing—Original Draft, M.J.G.A.; Writing—Review and Editing, M.J.G.A. and M.A.L.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico, Brazil, Grant Numbers 304107/2020-4, 306252/2021-0, 401896/2013-7 and 483287/2013-0; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil, Finance Code 001 and Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco, Brazil, Grant Numbers BCT-0406-5.03/21, APQ-0453-5.01/15 and BPV-0008-5.01/19.

Data Availability Statement

Data are available upon request to contact author.

Acknowledgments

We acknowledge the Instituto Agronômico de Pernambuco for overall support through several staff members.

Conflicts of Interest

The authors declare no conflict of interest.

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Plants 12 02589 g001 550
Figure 1. Number of pangolão grass endophytic bacteria positive for growth in N-free media (a) or presenting given percentiles of IAA synthesis (b), siderophore production (c), and calcium phosphate solubilization (d).
Figure 1. Number of pangolão grass endophytic bacteria positive for growth in N-free media (a) or presenting given percentiles of IAA synthesis (b), siderophore production (c), and calcium phosphate solubilization (d).
Plants 12 02589 g001
Plants 12 02589 g002 550
Figure 2. Pangolão grass endophytic bacteria grouped by in vitro growth promotion mechanisms. N—growth in N-free media; I—IAA production; S—siderophore production; P—calcium phosphate solubilization; +—bacteria presents the trait; −—bacteria does not present the trait.
Figure 2. Pangolão grass endophytic bacteria grouped by in vitro growth promotion mechanisms. N—growth in N-free media; I—IAA production; S—siderophore production; P—calcium phosphate solubilization; +—bacteria presents the trait; −—bacteria does not present the trait.
Plants 12 02589 g002
Table
Table 1. Growth performance of maize inoculated with pangolão endophytic bacteria under restricted N availability.
Table 1. Growth performance of maize inoculated with pangolão endophytic bacteria under restricted N availability.
TreatmentsPH (cm)CD (mm)LASDMRDMSANSAPRECIRENRE + C
(cm2)(mg)mg Plant−1 %
14C73 *4.882 *1029788878198 *7956
212B265 *5.377 *1113655 *898218 *8661
252A65 *594895506 *9091726949
333B614.882 *759528 *5681815841
338A60487 *8614368791666647
36D67 *5.191 *817566 *9471576344
389B65 *5.798 *661583 *6151275136
394D72 *5.591 *994668 *858191 *7654
396B71 *5.9 *116968563857186 *7553
432D71 *5.497 *1078759997207 *8359
503868 *570890694 *7971716948
5038A644.8103856745 *6891666647
5057A66 *5.498911524 *6581757050
521169 *5.710711017661078212 *8560
529767 *5.3108838706 *7371616446
534772 *5.81231073501 *10011 *206 *8358
5358A68 *5.391 *939667 *8671817251
N1C65 *4.692894674 *8781726949
N27D635.185 *874568 *7871686748
N37C624.579 *668543 *8831245136
+C73 *6.7 *1281786 *1543158 *19274 *137 *97 *
NI70 *599 *1261 *86710810 *242 *97 *69 *
CI534.548498225615933827
CV1.75.933.53.94.814.53.95.66.1
SDE0.030.040.060.100.110.090.130.090.100.10
+C = Application of 100% of the recommended dose; NI = no inoculation; CI = commercial inoculant; PH = plant height; CD = colm diameter; LA = leaf area; SDM = shoot dry mass; RDM = dry mass of the root system; SAN = accumulation of N in the aerial part; SAP = accumulation of P in the aerial part; RECI = efficiency relative to the commercial inoculant; REN = non-inoculated control relative efficiency; RE + C = relative efficiency positive control. CV = coefficient of variation. SDE = residual standard deviation. RDM, SDM, SAN, SAP, RER, REN, and RE + C data were log10 transformed. Means followed by an asterisk differ significantly from inoculation with the recommended strain at 0.05 probability by Dunnett’s test.
Table
Table 2. Growth performance of maize inoculated with pangolão endophytic bacteria under restricted water availability.
Table 2. Growth performance of maize inoculated with pangolão endophytic bacteria under restricted water availability.
TreatmentsPH (cm)CD (mm)LASDMRDMSANSAPRECIRENRE + C
(cm2)(mg)mg Plant−1 %
121B1584.566556891376 *97101102
192C604.173564664465100104106
212B2594.37656086636499104105
230A654.374718595353127133134
289A604.475465579374838687
303A2594.674626813466 *109114115
333B654.985702613384125130131
335C71 *5.4 *7464280359 *6114119120
338A606.5106727939 *86 *5 *108113114
402B605.2 *727001066 *1237 *124130131
415A564.953614798414109114115
425B514.464496993 *57 *3889293
432D604.276585657332104108109
5038615100688898343122127129
5038A644.61041140 *1450434202 *211 *213 *
5095564.149455911 *324788182
5155583.570499784435 *929697
5211634.276572766403101106107
5276604.581659803434145 *151 *153 *
5287654.658633750364112117119
528967 *4.972804859444140 *146 *148 *
5347635.178661907495117122124
5358A68 *4.981821 *1010 *77 *8146 *152 *154 *
+C544.65547026177 *6 *808485
N42A604.27757967061 *3103107108
NI564.7745051149 *464727576
CI55474432384283757979
CV1.76.24.13.43.86.214.4444
SDE0.030.040.080.100.110.100.090.080.080.08
+C = 100% pot-water holding capacity; NI = no inoculation; CI = commercial inoculant; PH = plant height; CD = colm diameter; LA = leaf area; SDM = shoot dry mass; RDM = dry mass of the root system; SAN = accumulation of N in the aerial part; SAP = accumulation of P in the aerial part; RECI = efficiency relative to the commercial inoculant; REN = non-inoculated control relative efficiency; RE + C = relative efficiency positive control. CV = coefficient of variation. SDE = residual standard deviation. Height, LA, SDM, RDM, SAN, and SAP data were transformed in to log10. Means followed by an asterisk differ significantly from inoculation with the recommended strain at 0.05 probability by Dunnett’s test.
Table
Table 3. Growth performance of maize inoculated with pangolão endophytic bacteria with low solubility P.
Table 3. Growth performance of maize inoculated with pangolão endophytic bacteria with low solubility P.
TreatmentsPH (cm)CD (mm)LASDMRDMSANSAPRECIRENRE + C
(cm2)(mg)mg Plant−1%
252A765.61201318932619140140146
333B86 *5.6157 *13151177959140139146
334C1816.11341558133912513165165173
335C747.4 *12315651441 *1389166166174
347B715.21041002122010713 *106106111
377D796.614716552791877176175184
389B555.310653864211915 *109109114
396B90 *6.111814481026716154153161
413D2775.810013702131 *978145145152
41C795.7121130012659010138138144
432D795.410112989331168138138144
5038746.212112755931008135135142
5057A96 *6.513919661631 *10615 *209208218
5095725.410610311029827109109115
5211795.511711231117677119119125
5347735.110711738121118128128134
G20745.710213841413 *11916 *147147154
N37C757 *168 *13591564 *12215 *144144151
N40E715.68812271595 *1129130130136
N5G877.312617141510 *16315 *182182190
N9B766.212213051016889139138145
+C665.2828762016 *696939397
NI795.6114943911818100100105
CI665959316148759999103
CV26.63.65.44.48.414.56.36.36.3
SDE0.040.050.070.160.140.170.140.140.140.14
+C = recommended dose of P2O5 provided by triple superphosphate; NI = no inoculation; CI = commercial inoculant; PH = plant height; CD = colm diameter; LA = leaf area; SDM = shoot dry mass; RDM = dry mass of the root system; SAN = accumulation of N in the aerial part; SAP = accumulation of P in the aerial part; RECI = efficiency relative to the commercial inoculant; REN = non-inoculated control relative efficiency; RE + C = relative efficiency positive control. CV = coefficient of variation. SDE = residual standard deviation. All data were transformed by log10. Means followed by an asterisk differ significantly from the commercial inoculant control at 0.05 probability, by Dunnett’s test.
Table
Table 4. Pearson’s correlation between in vitro growth promoting characteristics of the strains and results obtained in the BNF, IAA, siderophore, and phosphate solubilization experiments.
Table 4. Pearson’s correlation between in vitro growth promoting characteristics of the strains and results obtained in the BNF, IAA, siderophore, and phosphate solubilization experiments.
PHCDLASDMRDMSANSAPRECIRENRE + C
BNF
SI−0.242−0.125−0.093−0.358 **−0.173−0.214−0.297 *−0.218−0.358 **−0.358 **
IAA−0.0150.169−0.154−0.096−0.110−0.172−0.091−0.058−0.096−0.096
Siderophore0.1820.2280.1430.0780.100−0.1330.0400.1130.0780.078
BNF−0.091−0.204−0.303 *−0.095−0.048−0.069−0.1550.024−0.095−0.095
IAA
SI−0.1340.012−0.128−0.090−0.1320.018−0.100−0.105−0.105−0.105
IAA−0.136−0.180−0.072−0.115−0.076−0.013−0.049−0.115−0.115−0.115
Siderophore−0.086−0.205−0.134−0.104−0.115−0.155−0.169−0.139−0.139−0.139
BNF0.0680.0530.0430.0590.0370.1020.0610.0640.0640.064
Siderophore
SI0.259 *0.0730.1340.2010.0100.0280.1040.2010.2010.201
IAA0.1600.0810.1220.2160.0940.0270.1300.2160.2160.216
Siderophore0.145−0.045−0.1320.058−0.003−0.051−0.1490.0580.0580.058
BNF−0.008−0.0190.0730.0020.062−0.0430.0330.0020.0020.002
Phosphate Solubilization
SI−0.1670.096−0.073−0.0090.309 *0.0290.072−0.047−0.047−0.047
IAA−0.083−0.165−0.212−0.0150.068−0.0140.094−0.075−0.075−0.075
Siderophore−0.121−0.221−0.159−0.126−0.229−0.080−0.028−0.167−0.167−0.167
BNF−0.0840.1190.0290.0550.1390.1260.1360.0070.0070.007
All data were transformed by log10. * and ** significant at 5% and 1% probability, respectively. SI = phosphate solubilization index. PH = plant height; CD = colm diameter; LA = leaf area; SDM = shoot dry mass; RDM = dry mass of the root system; SAN = accumulation of N in the aerial part; SAP = accumulation of P in the aerial part; RECI = efficiency relative to the commercial inoculant; REN = non-inoculated control relative efficiency; RE + C = relative efficiency positive control.
Table
Table 5. Pangolão endophytic bacteria, grouped according to their in vitro growth promotion mechanisms performance, and their effects on maize growth under different environmental stresses, reduced N availability, water deficit stress, low P solubility, and low Fe solubility.
Table 5. Pangolão endophytic bacteria, grouped according to their in vitro growth promotion mechanisms performance, and their effects on maize growth under different environmental stresses, reduced N availability, water deficit stress, low P solubility, and low Fe solubility.
PHCDLASDMRDMSANSAPRECIRENRE + C
BNF
BNF
+66a5a86b871a628a80a7a172a67a47a
−67a5a97a919a607a83a8a177a71a50a
SI
0–7568a5a94a928a631a83a8a179a71a50a
75–9563a5ab88a824a517a71a8ab177a63a45a
95–10062a4b80a668a541a88a3b124a51a36a
IAA
5–2566a5a90a919a643a81a8a177a71a50a
25–5067a5a99a899a613a87a7a172a69a49a
50–7566a5a90a850a582a75a7a170a65a46a
75–9069a5a84a1054a661a87a8a204a81a57a
Siderophore
0–564a5a89a839a498a90a8a161a65a46a
5–2566a5a91a908a584a76a7a175a70a49a
25–5066a5a92a808a590a83a6a154a62a44a
CV1.75.92.93.43.94.614.43.95.45.9
SDE0.030.030.060.100.110.090.120.090.100.10
IAA
BNF
+60a5a75a614a832a43b4b108a112a113a
−63a5a73a664a795a53a5a122a127a128a
SI
0–7561a5a76a662a846a47a4a118a123a124a
75–9559a4a74a550ab696a44a4a98b102b103b
95–10063a5a60a534b857a43a5a94b98b99b
IAA
5–2563a5a90a831a1101a79a6a141a147a149a
25–5064a5a76a611b778b44bc4b109ab114ab115ab
50–7559ab5a68a605b796ab36c4b107ab111ab112ab
75–9062ab4b70a630b749b38bc4b112ab116ab118ab
Siderophore
0–563a5a80ab630a876a57a6a106a111a119a
5–2562a5a73ab683a880a59a6a126a132a108a
25–5058a4b67ab580a754b41b4b103a108a97a
50–7561a4b76ab570a763b45ab3b101a106a85a
75–9563a5a85a717a844a41b4b127a132a103a
95–10058a4b60b505a779b38b4b88a92a88a
CV1.7643.23.85.8144.14.14.1
SDE0.030.040.080.090.110.100.090.090.090.09
Siderophore
BNF
+73a6a108a1273a827a98a8a87a99a117a
−72a6a113a1299a903a94a8a88a101a120a
SI
0–7571b6a107b1211b807b94a8a82b94b112b
75–9578a6a109ab1458a1012a110a10a99a113a134a
95–10076a6a118a1384ab814ab98a8a94ab107ab128ab
IAA
5–2568b6a106ab1097b693a88a8a75b85b101b
25–5075a6a115a1287ab849a97a9a87ab100ab119ab
50–7575a6a108ab1348a896a103a9a92a105a124a
75–9072ab6a114ab1433a888a98a8a97a111a132a
Siderophore
0–569b6a113ab1111b692b94a9ab76b86b102b
5–2572b6a113ab1258ab966a93a8a86ab98ab116ab
25–5080a6a119a1540a1017a123a10a105a119a142a
50–7572b6a102b1277ab835ab89a7b87ab99ab118ab
75–9572b6a108ab1253ab752ab96a10a85ab97ab116ab
95–10074ab6a99b1259ab819ab91a7b86ab98ab116ab
CV1.762.32.33.55.910.73.73.63.5
SDE0.030.050.050.070.100.120.100.070.070.07
Phosphate Solubilization
BNF
+77a6a117a1267a1145a97a9a141a140a147a
−76a6a124a1354a1401b111a11a144a143a150a
SI
0–7577a6a115a1183a916b96a9a138a138a144a
75–9580a6a129a1389a1378ab100a11a148a147a154a
95–10074a6a113a1311a1414a107a10a139a139a146a
IAA
5–2581a7a124a1496a1239ab120a12a159a158a146a
25–5075a6a122a1209a1170b101a9a139a139a166a
50–7578a6a120a1307a1151b95a10a139a139a145a
75–9075a6a101a1377a1735a107a11a146a146a153a
Siderophore
0–574a7a123a1565a1441a138a9a166a166a174a
5–2581a6a130a1501a1651a105a12a159a159a167a
25–5073a6a117a1143a1151a98a10a135a134a141a
50–7579a5a117a1123a1117a67a7a119a119a125a
75–9579a6a115a1348a1102b107a10a144a143a150a
95–10074a6a113a1160a1022b85a8a123a123a129a
CV1.96.83.45.34.18.313.26.16.16.1
SDE0.040.050.070.170.130.170.130.130.130.13
Means followed by the same letter do not differ statistically from each other, lowercase in the column, at 0.05 probability, by Tukey’s test. PH = plant height; CD = colm diameter; LA = leaf area; SDM = shoot dry mass; RDM = dry mass of the root system; SAN = accumulation of N in the aerial part; SAP = accumulation of P in the aerial part; RECI = efficiency relative to the commercial inoculant; REN = non-inoculated control relative efficiency; RE + C = relative efficiency positive control. CV = coefficient of variation. SDE = residual standard deviation.
Table
Table 6. Strains selected for the maize growth-promotion experiments. BNF—reduced N availability, IAA—water deficit stress, P—low P solubility, and Siderophore—low Fe solubility. Grey cells indicate those in common to all experiments. + and - indicate presence or absence of the trait, respectively.
Table 6. Strains selected for the maize growth-promotion experiments. BNF—reduced N availability, IAA—water deficit stress, P—low P solubility, and Siderophore—low Fe solubility. Grey cells indicate those in common to all experiments. + and - indicate presence or absence of the trait, respectively.
StrainClassificationBNFIAAPSiderophore
5038 ++++
5095Enterobacter-+++
5155Rhizobium-+--
5211Stenotrophomonas++++
5227Pseudomonas---+
5276Rhizobium-+--
5287Stenotrophomonas-+-+
5289 -+--
5297Rhizobium+--+
5347Stenotrophomonas++++
5410Rhizobium---+
121B1Ochrobactrum-+-+
14CVariovorax+---
192CAchromobacter-+-+
212B2Rhizobium++-+
230ARhizobium-+--
231B1Priestia---+
252APantoea+-++
289A -+--
303A2Agrobacterium-+--
331CRhizobium---+
333BPantoea++++
334C1Pantoea--+-
335CRhizobium-+++
338ARhizobium++-+
344BRhizobium---+
347BStenotrophomonas--+-
36DStenotrophomonas+---
377DPantoea--+-
389BPantoea+-+-
394DRhizobium+---
396B +-++
402B -+--
413D2Ochrobactrum--++
415APantoea-+--
41CEnterobacter--+-
425BRhizobium-+--
432DStenotrophomonas++++
5038APantoea++--
5057AShinella+-++
5358APaenibacillus++-+
G20Enterobacter--+-
N1CVariovorax+---
N27DPseudomonas+---
N37C +-+-
N40E --+-
N42AAgrobacterium-+--
N5GBurkholderia--+-
N9BBurkholderia--++
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Alves, M.J.G.; Mendonça, J.J.; Vitalino, G.M.; Oliveira, J.P.; Carvalho, E.X.; Fracetto, F.J.C.; Fracetto, G.G.M.; Lira Junior, M.A. Screening Digitaria eriantha cv. Suvernola Endophytic Bacteria for Maize Growth Promotion. Plants 2023, 12, 2589. https://doi.org/10.3390/plants12142589

AMA Style

Alves MJG, Mendonça JJ, Vitalino GM, Oliveira JP, Carvalho EX, Fracetto FJC, Fracetto GGM, Lira Junior MA. Screening Digitaria eriantha cv. Suvernola Endophytic Bacteria for Maize Growth Promotion. Plants. 2023; 12(14):2589. https://doi.org/10.3390/plants12142589

Chicago/Turabian Style

Alves, Michelle J. G., Johny Jesus Mendonça, Gisely Moreira Vitalino, José Paula Oliveira, Erix Xavier Carvalho, Felipe José Cury Fracetto, Giselle Gomes Monteiro Fracetto, and Mario Andrade Lira Junior. 2023. "Screening Digitaria eriantha cv. Suvernola Endophytic Bacteria for Maize Growth Promotion" Plants 12, no. 14: 2589. https://doi.org/10.3390/plants12142589

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