Halotolerant Bacterial Diversity Associated with Suaeda fruticosa (L.) Forssk. Improved Growth of Maize under Salinity Stress
Abstract
:1. Introduction
2. Materials and Methods
2.1. Isolation of Bacterial Strains
2.2. 16S rRNA Gene Sequencing
2.3. Halophility Assay
2.4. Plant-Growth-Promoting Traits
2.5. Biofilm Formation
2.6. In Vitro Plant Bioassay
2.7. Pot Trials with Salt Stress
2.8. Biochemical Analysis of Plants
2.9. Statistical Analysis
3. Results
3.1. Strains Identification
3.2. Halophility Assay
3.3. Plant-Growth-Promoting Traits
3.4. In Vitro Plant Bioassay
3.5. Pot Trials under Salt Stress
3.6. Antioxidant Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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S. No. | Strains | Identified as | Accessions |
---|---|---|---|
1 | F-1 | Gracilibacillus saliphilus F-1 | KT027652 |
2 | F-2 | Staphylococcus petrasii F-2 | KT027653 |
3 | F-3 | Virgibacillus salarius F-3 | KT027654 |
4 | F-4 | G. saliphilus F-4 | KT027655 |
5 | F-5 | Salinicoccus sesuvii F-5 | KT027656 |
6 | F-6 | Bacillus licheniformis F-6 | KT027657 |
7 | F-7 | B. subtilis F-7 | KT027658 |
8 | F-8 | B. mojavensis F-8 | KT027659 |
9 | F-9 | Zhihengliuella flava F-9 | KT027660 |
10 | F-10 | B. licheniformis F-10 | KT027661 |
11 | F-11 | S. jettensis F-11 | KT027662 |
12 | F-12 | S. arlettae F-12 | KT027663 |
13 | F-13 | B. sonorensis F-13 | KT027664 |
14 | F-14 | B. subtilis F-14 | KT027665 |
15 | F-15 | B. aerius F-15 | KT027666 |
16 | F-16 | B. licheniformis F-16 | KT027667 |
17 | F-17 | B. subtilis F-17 | KT027668 |
18 | F-18 | B. atrophaeus F-18 | KT027669 |
19 | F-19 | Brevibacterium halotolerans F-19 | KT027670 |
20 | F-20 | B. subtilis F-20 | KT027671 |
21 | F-21 | B. licheniformis F-21 | KT027672 |
22 | F-22 | B. axarquiensis F-22 | KT027673 |
23 | F-23 | B. amyloliquefaciens F-23 | KT027674 |
24 | F-24 | B. subtilis F-24 | KT027675 |
25 | F-25 | B. subtilis F-25 | KT027676 |
26 | F-26 | G. thailandensis F-26 | KT027677 |
27 | F-27 | B. subtilis F-27 | KT027678 |
28 | F-28 | Oceanobacillus picturae F-28 | KT027679 |
29 | F-29 | S. devriesei F-29 | KT027680 |
30 | F-30 | S. jettensis F-30 | KT027681 |
31 | F-31 | S. petrasii F-31 | KT027682 |
32 | F-32 | B. subtilis F-32 | KT027683 |
33 | F-33 | B. infantis F-33 | KT027684 |
34 | F-34 | B. subtilis F-32 | KT027685 |
35 | F-35 | Exiguobacterium mexicanum F-35 | KT027686 |
36 | F-36 | B. subtilis F-36 | KT027687 |
37 | F-37 | S. caprae F-37 | KT027688 |
38 | F-38 | S. devriesei F-38 | KT027689 |
39 | F-39 | S. hominis F-39 | KT027690 |
40 | F-83 | B. stratosphericus F-83 | KT027734 |
41 | F-84 | B. pumilus F-84 | KT027735 |
42 | F-85 | B. pumilus F-85 | KT027736 |
43 | F-86 | B. marisflavi F-86 | KT027737 |
44 | F-87 | Pseudomonas japonica F-87 | KT027738 |
45 | F-89 | Sal. sesuvii F-89 | KT027740 |
S. No. | Strains | Identified as | Accessions |
---|---|---|---|
1 | F-40 | Bacillus subtilis F-40 | KT027691 |
2 | F-41 | Exiguobacterium sp. F-41 | KT027692 |
3 | F-42 | Staphylococcus jettensis F-42 | KT027693 |
4 | F-43 | Salinicoccus sesuvii F-43 | KT027694 |
5 | F-44 | Oceanobacillus kapialis F-44 | KT027695 |
6 | F-45 | B. flexus F-45 | KT027696 |
7 | F-46 | B. pumilus F-46 | KT027697 |
8 | F-47 | S. devriesei F-47 | KT027698 |
9 | F-48 | B. malacitensis F-48 | KT027699 |
10 | F-49 | B. malacitensis F-49 | KT027700 |
11 | F-50 | E. aquaticum F-50 | KT027701 |
12 | F-51 | O. polygoni F-51 | KT027702 |
13 | F-52 | O. kimchii F-52 | KT027703 |
14 | F-53 | B. mojavensis F-53 | KT027704 |
15 | F-54 | B. megaterium F-54 | KT027705 |
16 | F-55 | B. pumilus F-55 | KT027706 |
17 | F-56 | Sal. roseus F-56 | KT027707 |
18 | F-57 | B. subtilis F-57 | KT027708 |
19 | F-58 | B. megaterium F-58 | KT027709 |
20 | F-59 | B. aryabhattai F-59 | KT027710 |
21 | F-60 | B. tequilensis F-60 | KT027711 |
22 | F-61 | B. malacitensis F-61 | KT027712 |
23 | F-62 | B. subtilis F-62 | KT027713 |
24 | F-63 | S. warneri F-63 | KT027714 |
25 | F-64 | Arthrobacter bergerei F-64 | KT027715 |
26 | F-65 | A. ardleyensis F-65 | KT027716 |
27 | F-66 | A. arilaitensis F-66 | KT027717 |
28 | F-67 | B. subtilis F-67 | KT027718 |
29 | F-68 | B. cereus F-68 | KT027719 |
30 | F-69 | S. arlettae F-69 | KT027720 |
31 | F-70 | S. cohnii F-70 | KT027721 |
32 | F-71 | S. arlettae F-71 | KT027722 |
33 | F-72 | S. jettensis F-72 | KT027723 |
34 | F-73 | Pseudomonas rhizosphaerae F-73 | KT027724 |
35 | F-74 | S. gallinarum F-74 | KT027725 |
36 | F-75 | S. petrasii F-75 | KT027726 |
37 | F-76 | S. lugdunensis F-76 | KT027727 |
38 | F-77 | S. capitis F-77 | KT027728 |
39 | F-78 | S. pasteuri F-78 | KT027729 |
40 | F-79 | S. jettensis F-79 | KT027730 |
41 | F-80 | S. equorum F-80 | KT027731 |
42 | F-81 | Halomonas nanhaiensis F-81 | KT027732 |
43 | F-82 | B. safensis F-82 | KT027733 |
44 | F-88 | O. kimchii F-88 | KT027739 |
45 | F-90 | E. mexicanum F-90 | KT027741 |
46 | F-91 | Exiguobacterium sp. F-91 | KT027742 |
S. No. | Strains | l-tryptophan (µg mL−1) | |
---|---|---|---|
0 | 500 | ||
Auxin (µg mL−1) | |||
1 | Gracilibacillus saliphilus F-1 | 6.20 (a) | 15.70 (a) |
2 | Staphylococcus petrasii F-2 | 9.30 (a) | 113.50 (o) |
3 | Virgibacillus salarius F-3 | 87.90 (i) | 150.00 (p) |
4 | Zhihengliuella flava F-9 | 44.70 (d–h) | 215.00 (r) |
5 | S. jettensis F-11 | 63.20 (g–i) | 185.70 (qr) |
6 | S. arlettae F-12 | 51.40 (e–i) | 174.30 (pq) |
7 | Exiguobacterium sp. F-41 | 6.40 (a) | 43.50 (a–f) |
8 | S. jettensis F-42 | 33.60 (d–g) | 78.70 (l–o) |
9 | Salinicoccus sesuvii F-43 | 16.50 (abc) | 28.40 (abc) |
10 | S. devriesei F-47 | 78.30 (hi) | 28.00 (abc) |
11 | Bacillus megaterium F-58 | 20.80 (abc) | 48.70 (a–g) |
12 | B. aryabhattai F-59 | 25.90 (d–g) | 61.20 (i–n) |
13 | S. warneri F-63 | 6.40 (a) | 14.00 (a) |
14 | Arthrobacter bergerei F-64 | 13.40 (ab) | 25.50 (abc) |
15 | A. ardleyensis F-65 | 9.10 (a) | 29.60 (abc) |
16 | S. arlettae F-69 | 14.30 (abc) | 54.20 (h–n) |
17 | S. cohnii F-70 | 15.70 (abc) | 42.10 (a–f) |
18 | S. arlettae F-71 | 53.60 (f–i) | 88.60 (no) |
19 | S. jettensis F-72 | 30.60 (d–g) | 59.80 (i–n) |
20 | Pseudomonas rhizosphaerae F-73 | 36.80 (d–g) | 67.70 (g–n) |
21 | S. gallinarum F-74 | 15.40 (abc) | 23.00 (abc) |
22 | S. pasteuri F-78 | 10.40 (a) | 36.90 (a–c) |
23 | S. jettensis F-79 | 5.70 (a) | 24.50 (abc) |
24 | S. equorum F-80 | 7.60 (a) | 32.20 (a–d) |
25 | Halomonas nanhaiensis F-81 | 21.10 (abc) | 83.30 (mno) |
26 | B. safensis F-82 | 9.50 (a) | 43.90 (a–f) |
27 | B. stratosphericus F-83 | 23.60 (def) | 72.70 (k–n) |
28 | B. pumilus F-84 | 7.90 (a) | 18.10 (ab) |
29 | B. pumilus F-85 | 32.60 (a–d) | 59.80 (i–n) |
30 | B. marisflavi F-86 | 22.60 (abc) | 38.60 (a–e) |
Strains | Shoot Length (cm) | Root Length (cm) | Roots/Plant | Fresh Weight (g) | Dry Weight (g) |
---|---|---|---|---|---|
Control | 23 (a) | 13 (b) | 6.4 (de) | 4.6 (a) | 0.7 (ab) |
F-9 | 28 (bcd) | 20 (cd) | 4.8 (a) | 5.3 (ab) | 0.9 (abc) |
F-11 | 32 (defg) | 20 (cde) | 5.6 (abcd) | 6.8 (a–e) | 1.1 (bc) |
F-12 | 34 (fgh) | 25 (f) | 6.2 (bcde) | 8.8 (ef) | 1.3 (c) |
F-35 | 31 (c–g) | 21 (de) | 5.7 (abcd) | 5.7 (abc) | 0.8 (ab) |
F-37 | 29 (cd) | 20 (cde) | 5.5 (abcd) | 10.2 (f) | 0.9 (abc) |
F-58 | 33 (efgh) | 20 (cde) | 6.0 (bcd) | 7.4 (b–f) | 0.9 (abc) |
F-71 | 34 (gh) | 22 (def) | 5.7 (abcd) | 8.1 (cdef) | 1.1 (bc) |
F-72 | 37 (h) | 24 (f) | 7.1 (e) | 7.8 (b–f) | 1.0 (abc) |
F-81 | 30 (cdef) | 20 (cd) | 5.0 (ab) | 7.5 (b–f) | 1.3 (c) |
F-83 | 29 (cde) | 23 (ef) | 6.2 (cde) | 4.2 (a) | 0.6 (a) |
F-84 | 31 (c–g) | 22 (def) | 5.1 (abc) | 6.0 (abcd) | 1 (abc) |
F-87 | 28 (bc) | 19 (cd) | 5.4 (abcd) | 8.6 (def) | 1.1 (bc) |
* C-1 | 22 (a) | 10 (a) | 5.6 (abcd) | 9.1 (ef) | 1.1 (bc) |
* C-2 | 24 (ab) | 14 (b) | 6.5 (de) | 7.8 (b–f) | 1.3 (c) |
* C-3 | 23 (a) | 17 (c) | 5.6 (abcd) | 10.1 (f) | 1.4 (ab) |
Strains | NaCl (mM) | Shoot Length (cm) | Root Length (cm) | Roots/Plant | Fresh Weight (g) | Dry Weight (g) |
---|---|---|---|---|---|---|
Control | 0 | 22 (b–g) | 13 (abc) | 5.0 (jklm) | 0.9 (abcd) | 0.1 (a) |
200 | 22 (bcde) | 16 (bcde) | 4.2 (i–m) | 1.2 (c–j) | 0.1 (abcd) | |
400 | 14 (a) | 13 (abc) | 4.3 (a–e) | 1.1 (c–g) | 0.1 (ab) | |
F-9 | 0 | 29 (i–o) | 19 (e–k) | 5.0 (b–j) | 2.0 (r) | 0.3 (e–l) |
200 | 29 (i–p) | 21 (g–n) | 5.2 (b–l) | 1.7 (pqr) | 0.2 (abcd) | |
400 | 25 (d–i) | 21 (f–m) | 4.6 (a–f) | 1.6 (l–q) | 0.2 (c–h) | |
F-11 | 0 | 32 (n–s) | 20 (e–k) | 6.0 (e–l) | 1.8 (qr) | 0.4 (nop) |
200 | 35 (rs) | 25 (m) | 6.0 (f–l) | 1.6 (m–r) | 0.4 (op) | |
400 | 32 (n–r) | 24 (klmn) | 5.0 (b–k) | 1.6 (n–r) | 0.2 (e–j) | |
F-12 | 0 | 34 (pqrs) | 25 (mn) | 6.2 (h–m) | 1.6 (n–r) | 0.3 (j–p) |
200 | 34 (pqrs) | 23 (j–n) | 6.0 (f–m) | 1.4 (g–n) | 0.3 (d–j) | |
400 | 30 (k–r) | 22 (h–n) | 6.3 (jklm) | 1.3 (f–l) | 0.3 (e–k) | |
F-35 | 0 | 31 (l–r) | 21 (g–n) | 6.0 (f–l) | 1.5 (j–p) | 0.2 (c–h) |
200 | 26 (f–l) | 21 (g–n) | 6.4 (klm) | 1.2 (c–i) | 0.2 (c–g) | |
400 | 25 (e–i) | 21 (g–m) | 5.0 (b–j) | 1.0 (b–f) | 0.2 (e–j) | |
F-37 | 0 | 29 (i–o) | 20 (f–l) | 5.5 (e–l) | 1.0 (a–e) | 0.4 (k–p) |
200 | 27 (g–m) | 21 (g–n) | 5.3 (b–l) | 0.7 (ab) | 0.1 (abc) | |
400 | 23 (b–g) | 16 (bcde) | 5.1 (b–k) | 1.4 (g–n) | 0.3 (i–o) | |
F-58 | 0 | 33 (o–s) | 21 (f–m) | 6.0 (g–m) | 1.2 (d–k) | 0.3 (e–j) |
200 | 29 (i–o) | 21 (f–m) | 5.0 (b–i) | 1.7 (opqr) | 0.2 (c–i) | |
400 | 23 (b–g) | 21 (f–m) | 3.4 (a) | 1.1 (c–g) | 0.4 (l–p) | |
F-71 | 0 | 34 (qrs) | 22 (h–n) | 6.0 (f–l) | 1.4 (h–p) | 0.3 (f–m) |
200 | 33 (o–s) | 23 (j–n) | 6.0 (g–m) | 1.5 (l–q) | 0.3 (e–k) | |
400 | 23 (c–h) | 18 (d–i) | 5.0 (b–i) | 1.5 (k–p) | 0.3 (g–m) | |
F-72 | 0 | 37 (s) | 24 (lmn) | 7.1 (m) | 1.7 (opqr) | 0.3 (f–m) |
200 | 32 (n–r) | 18 (d–h) | 8.6 (n) | 1.6 (m–r) | 0.2 (c–h) | |
400 | 25 (e–i) | 21 (g–n) | 5.0 (b–h) | 1.3 (g–m) | 0.3 (i–o) | |
F-81 | 0 | 30 (i–q) | 19 (e–j) | 5.0 (b–k) | 1.4 (i–p) | 0.4 (p) |
200 | 28 (i–o) | 20 (f–l) | 5.0 (b–g) | 1.5 (j–p) | 0.2 (bcde) | |
400 | 20 (bcd) | 16 (cdef) | 4.6 (a–g) | 1.0 (b–f) | 0.1 (abc) | |
F-83 | 0 | 29 (i–o) | 23 (i–n) | 6.2 (i–m) | 1.0 (a–f) | 0.2 (c–g) |
200 | 29 (i–o) | 22 (g–n) | 5.5 (e–l) | 1.0 (abcd) | 0.2 (c–h) | |
400 | 21 (bcde) | 19 (e–k) | 4.6 (a–f) | 0.7 (a) | 0.2 (b–f) | |
F-84 | 0 | 31 (m–r) | 22 (h–n) | 5.1 (b–k) | 1.1 (c–g) | 0.2 (d–j) |
200 | 28 (i–n) | 18 (d–h) | 5.0 (b–i) | 1.1 (c–g) | 0.2 (b–f) | |
400 | 20 (bcd) | 18 (d–h) | 4.1 (abcd) | 1.4 (g–o) | 0.3 (h–n) | |
F-87 | 0 | 28 (i–n) | 19 (e–j) | 5.4 (d–l) | 1.2 (c–h) | 0.2 (d–j) |
200 | 32 (n–s) | 22 (g–n) | 6.0 (f–m) | 1.2 (e–l) | 0.3 (e–l) | |
400 | 28 (h–n) | 20 (f–l) | 5.0 (b–k) | 1.4 (g–n) | 0.3 (e–j) | |
* C-1 | 0 | 22 (b–f) | 10 (a) | 6.0 (e–l) | 1.3 (f–l) | 0.2 (c–h) |
200 | 19 (bc) | 12 (ab) | 5.2 (b–l) | 1.4 (g–n) | 0.2 (b–f) | |
400 | 25 (e–i) | 18 (d–h) | 4.0 (ab) | 1.6 (m–r) | 0.4 (mnop) | |
* C-2 | 0 | 24 (d–i) | 14 (abcd) | 6.5 (lm) | 1.4 (g–n) | 0.2 (c–h) |
200 | 19 (b) | 15 (bcde) | 5.4 (c–l) | 1.4 (g–n) | 0.2 (c–g) | |
400 | 26 (e–k) | 15 (bcde) | 4.6 (a–f) | 1.4 (g–o) | 0.2 (c–h) | |
* C-3 | 0 | 23 (c–h) | 17 (defg) | 5.6 (e–l) | 1.1 (c–g) | 0.2 (abcd) |
200 | 22 (bcde) | 18 (d–h) | 4.6 (a–g) | 1.0 (abc) | 0.2 (c–g) | |
400 | 19 (bc) | 21 (f–m) | 4.0 (abc) | 1.2 (c–i) | 0.3 (i–o) |
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Aslam, F.; Ali, B. Halotolerant Bacterial Diversity Associated with Suaeda fruticosa (L.) Forssk. Improved Growth of Maize under Salinity Stress. Agronomy 2018, 8, 131. https://doi.org/10.3390/agronomy8080131
Aslam F, Ali B. Halotolerant Bacterial Diversity Associated with Suaeda fruticosa (L.) Forssk. Improved Growth of Maize under Salinity Stress. Agronomy. 2018; 8(8):131. https://doi.org/10.3390/agronomy8080131
Chicago/Turabian StyleAslam, Faiza, and Basharat Ali. 2018. "Halotolerant Bacterial Diversity Associated with Suaeda fruticosa (L.) Forssk. Improved Growth of Maize under Salinity Stress" Agronomy 8, no. 8: 131. https://doi.org/10.3390/agronomy8080131