Exogenous Streptomyces spp. enhance the drought resistance of naked oat (Avena nuda) seedlings by augmenting both the osmoregulation mechanisms and antioxidant capacities
Meixia Qiao A , Siyuan Lv A , Yuejing Qiao A B , Wen Lin A B , Zhiqiang Gao A B , Xiwang Tang C , Zhenping Yang A B * and Jie Chen A B *A
B
C
Abstract
Drought is a major obstacle to the development of naked oat industry. This work investigated mechanisms by which exogenous Streptomyces albidoflavus T4 and Streptomyces rochei D74 improved drought tolerance in naked oat (Avena nuda) seedlings. Results showed that in the seed germination experiment, germination rate, radicle and hypocotyl length of naked oat seeds treated with the fermentation filtrate of T4 or D74 under PEG induced drought stress increased significantly. In the hydroponic experiment, the shoot and root dry weights of oat seedlings increased significantly when treated with the T4 or D74 fermentation filtrate under the 15% PEG induced drought stress (S15). Simultaneously, the T4 treatment also significantly increased the surface area, volume, the number of tips and the root activity of oat seedlings. Both T4 and D74 treatments elicited significant increases in proline and soluble sugar contents, as well as the catalase and peroxidase activities in oat seedlings. The results of comprehensive drought resistance capacity (CDRC) calculation of oat plants showed that the drought resistance of oat seedlings under the T4 treatment was better than that under the D74 treatment, and the effect was better under higher drought stress (S15). Findings of this study may provide a novel and effective approach for enhancing plant defenses against drought stress.
Keywords: antioxidase, drought resistance, drought stress, naked oat, osmoregulation, seed germination, seedling growth, Streptomyces.
References
Adegboye MF, Babalola OO (2015) Evaluation of antibiotic biosynthetic potential of actinomycete isolates to produce antimicrobial agents. British Microbiology Research Journal 7(5), 243-254.
| Crossref | Google Scholar |
Armada E, Probanza A, Roldán A, Azcón R (2016) Native plant growth promoting bacteria Bacillus thuringiensis and mixed or individual mycorrhizal species improved drought tolerance and oxidative metabolism in Lavandula dentata plants. Journal of Plant Physiology 192, 1-12.
| Crossref | Google Scholar | PubMed |
Ashrafi M, Azimi-Moqadam M-R, Moradi P, MohseniFard E, Shekari F, Kompany-Zareh M (2018) Effect of drought stress on metabolite adjustments in drought tolerant and sensitive thyme. Plant Physiology and Biochemistry 132, 391-399.
| Crossref | Google Scholar | PubMed |
Bakhoum GS, Sadak MS, Thabet MS (2023) Induction of tolerance in groundnut plants against drought stress and Cercospora leaf spot disease with exogenous application of arginine and sodium nitroprusside under field conditions. Journal of Soil Science and Plant Nutrition 23(4), 6612-6631.
| Crossref | Google Scholar |
Cao S, Wang W, Wang F, Zhang J, Wang Z, Yang S, Xue Q (2016) Drought-tolerant Streptomyces pactum Act12 assist phytoremediation of cadmium-contaminated soil by Amaranthus hypochondriacus: great potential application in arid/semi-arid areas. Environmental Science and Pollution Research 23(15), 14898-14907.
| Crossref | Google Scholar | PubMed |
Caplan JS, Meiners SJ, Flores-Moreno H, McCormack ML (2019) Fine-root traits are linked to species dynamics in a successional plant community. Ecology 100(3), e02588.
| Crossref | Google Scholar | PubMed |
Carlson R, Tugizimana F, Steenkamp PA, Dubery IA, Hassen AI, Labuschagne N (2020) Rhizobacteria-induced systemic tolerance against drought stress in Sorghum bicolor (L.) Moench. Microbiological Research 232, 126388.
| Crossref | Google Scholar | PubMed |
Chandra P, Wunnava A, Verma P, Chandra A, Sharma RK (2021) Strategies to mitigate the adverse effect of drought stress on crop plants—influences of soil bacteria: a review. Pedosphere 31(3), 496-509.
| Crossref | Google Scholar |
Chen J, Qiao M, Yang Y, Gao Z, Yang Z, Lin W (2023) Exogenous Streptomyces spp. benefit naked oat growth under dry farming conditions by modifying rhizosphere bacterial communities. Applied Soil Ecology 189, 104946.
| Crossref | Google Scholar |
Duan XM, Zhao FY, Yan X, Xue QH, Li XX, Wen BJ, Jia LH, Yan H (2016) Construction of SPA7074-deficient mutant of biocontrol strain Streptomyces pactum Act12 and characterization of its secondary metabolites. Acta Microbiologica Sinica 56(12), 1883-1891.
| Google Scholar | PubMed |
Duan N, Li QH, Chen XN, Gao JL, Duo PZ, Zhang RH, Wang JI (2019) Combined effects of simulated drought stress and nitrogen deposition on root growth characteristics of Nitraria tangutorum. Acta Agrestia Sinica 27(4), 956-961.
| Google Scholar |
Egorshina AA, Khairullin RM, Sakhabutdinova AR, Luk’yantsev MA (2012) Involvement of phytohormones in the development of interaction between wheat seedlings and endophytic Bacillus subtilis strain 11BM. Russian Journal of Plant Physiology 59(1), 134-140.
| Crossref | Google Scholar |
Gao W, Feng Z, Bai Q, He J, Wang Y (2019) Melatonin-mediated regulation of growth and antioxidant capacity in salt-tolerant naked oat under salt stress. International Journal of Molecular Sciences 20(5), 1176.
| Crossref | Google Scholar | PubMed |
Gao ZH, Li XY, Lan J, Hu HY (2022) Comparison and evaluation of seed germination indexes of different forage-type oat cultivars under PEG-6000 stress. Acta Agrestia Sinica 30(5), 1210-1218.
| Google Scholar |
Gao Y, Kou JC, Hou SQ, Lei TY, He HS, Wang P, Xie JY, Xiao JL (2023) Identification and screening of drought resistance of main spring soybean varieties in northeast China at seedling stage. Marine Pollution Bulletin 1-12.
| Google Scholar |
Hao R, Wang Z, Yang C, Deng Y, Zheng Z, Wang Q, Du X (2018) Metabolomic responses of juvenile pearl oyster Pinctada maxima to different growth performances. Aquaculture 491, 258-265.
| Crossref | Google Scholar |
Hatzig S, Zaharia LI, Abrams S, Hohmann M, Legoahec L, Bouchereau A, Nesi N, Snowdon RJ (2014) Early osmotic adjustment responses in drought-resistant and drought-sensitive oilseed rape. Journal of Integrative Plant Biology 56(8), 797-809.
| Crossref | Google Scholar | PubMed |
He Z, Cui K, Wang R, Xu T, Zhang Z, Wang X, Chen Y, Zhu Y (2023) Multi-omics joint analysis reveals how Streptomyces albidoflavus OsiLf-2 assists Camellia oleifera to resist drought stress and improve fruit quality. Frontiers in Microbiology 14, 1152632.
| Crossref | Google Scholar | PubMed |
Huang JP, Yu HP, Guan XD, Wang GY, Guo RX (2016) Accelerated dryland expansion under climate change. Nature Climate Change 6(2), 166-171.
| Crossref | Google Scholar |
Huang X-F, Zhou D, Lapsansky ER, Reardon KF, Guo J, Andales MJ, Vivanco JM, Manter DK (2017a) Mitsuaria sp. and Burkholderia sp. from Arabidopsis rhizosphere enhance drought tolerance in Arabidopsis thaliana and maize (Zea mays L.). Plant and Soil 419, 523-539.
| Crossref | Google Scholar |
Huang HG, Lv LX, Zhang YM, Jiang Z, Shen Y, An QL (2017b) Microbe-assisted drought resistance for tobacco plants: mechanisms and applications. Chinese Journal of Applied Ecology 28(9), 3099-3110.
| Google Scholar |
Huo KY, Luo C, Gao JJ, Zhang JX, Mo YQ, Zhang H, Tan JY (2023) Effects of exogeneous hormones on seed germination and seedling growth of Valeriana officinalis L. under drought stress. Shandong Agricultural Sciences 55(4), 65-72.
| Google Scholar |
Ji Y, Zhang XQ, Peng Y, Liang XY, Huang LK, Ma X, Ma YM (2014) Effects of drought stress on lipid peroxidation, osmoticad justment and activities of protective enzymes in the roots and leaves of orchardgrass. Acta Prataculturae Sinica 23(3), 144-151.
| Google Scholar |
Kaya C, Shabala S (2023) Melatonin improves drought stress tolerance of pepper (Capsicum annuum) plants via upregulating nitrogen metabolism. Functional Plant Biology 51, FP23060.
| Crossref | Google Scholar |
Khan AA, Rahmani AH, Aldebasi YH, Aly SM (2014) Biochemical and pathological studies on peroxidases – an updated review. Global Journal of Health Science 6(5), 87-98.
| Crossref | Google Scholar |
Kutasy E, Buday-Bódi E, Virág IC, Forgács F, Melash AA, Zsombik L, Nagy A, Csajbók J (2022) Mitigating the negative effect of drought stress in oat (Avena sativa L.) with silicon and sulphur foliar fertilization. Plants 11(1), 30.
| Crossref | Google Scholar |
Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant and Soil 200, 241-250.
| Crossref | Google Scholar |
Latt CR, Nair PKR, Kang BT (2001) Reserve carbohydrate levels in the boles and structural roots of five multipurpose tree species in a seasonally dry tropical climate. Forest Ecology and Management 146(1–3), 145-158.
| Crossref | Google Scholar |
Liu AR, Chen SC, Chen K, Lin XM, Wang FH (2010) Antagonism effect of Trichoderma harzianum against Fusarium oxysporum on cucumber and related genes expression analysis. Journal of Plant Protection 37(3), 249-254.
| Google Scholar |
Liu YT, Yang B, Zhang K, Ma JN, Wen HW, Lai HX, Xue QH (2020) Effect of seed coating with Streptomyces on panicle differentiation and biological characteristics of wheat. Journal of Triticeae Crops 40(8), 990-1001.
| Google Scholar |
Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiology 131(3), 1381-1390.
| Crossref | Google Scholar | PubMed |
Meier IC, Tückmantel T, Heitkötter J, Müller K, Preusser S, Wrobel TJ, Kandeler E, Marschner B, Leuschner C (2020) Root exudation of mature beech forests across a nutrient availability gradient: the role of root morphology and fungal activity. New Phytologist 226(2), 583-594.
| Crossref | Google Scholar | PubMed |
Okoro CK, Brown R, Jones AL, Andrews BA, Asenjo JA, Goodfellow M, Bull AT (2009) Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile. Antonie Van Leeuwenhoek 95(2), 121-133.
| Crossref | Google Scholar | PubMed |
Olanrewaju OS, Babalola OO (2019) Streptomyces: implications and interactions in plant growth promotion. Applied Microbiology and Biotechnology 103(3), 1179-1188.
| Crossref | Google Scholar | PubMed |
Peng YL, Zhang QS, Han LZ, Meng Y (2020) Screening for bacterial strains promoting seed germination of tobacco and study of their growth-promoting characteristics. Chinese Tobacco Science 41(5), 68-72.
| Google Scholar |
Qing C, Liu ZX, Li YJ (2023) Effect of compound microbial fertilizer AP on drought resistance of maize seedlings under drought stress by transcriptome analysis. Crops 1-10.
| Google Scholar |
Ren CZ, Cui L, Yang C, Tian CY, Fu XF, Liu YM, Zhao GQ, Guo L (2016) Establishment and application of hight efficient breeding technology system of oat in China. Journal of Agricultural Science and Technology 18(1), 1-6.
| Google Scholar |
Sadak MS (2023) Physiological role of Arbuscular Mycorrhizae and vitamin B1 on productivity and physio-biochemical traits of white lupine (Lupinus termis L.) under salt stress. Gesunde Pflanzen 75(5), 1885-1896.
| Crossref | Google Scholar |
Sadak MS, Bakry BA (2020) Alleviation of drought stress by melatonin foliar treatment on two flax varieties under sandy soil. Physiology and Molecular Biology of Plants 26(5), 907-919.
| Crossref | Google Scholar |
Sadak MS, Ramadan AAE-M (2021) Impact of melatonin and tryptophan on water stress tolerance in white lupine (Lupinus termis L.). Physiology and Molecular Biology of Plants 27(3), 469-481.
| Crossref | Google Scholar |
Saradhi PP (1991) Proline accumulation under heavy metal stress. Journal of Plant Physiology 138(5), 554-558.
| Crossref | Google Scholar |
Sati D, Pande V, Pandey SC, Samant M (2023) Recent advances in PGPR and molecular mechanisms involved in drought stress resistance. Journal of Soil Science and Plant Nutrition 23, 106-124.
| Crossref | Google Scholar |
Singh M, Sharma JG, Giri B (2023) Microbial inoculants alter resilience towards drought stress in wheat plants. Plant Growth Regulation 101, 823-843.
| Crossref | Google Scholar |
Sohrabi Y, Heidari G, Weisany W, Golezani KG, Mohammadi K (2012) Changes of antioxidative enzymes, lipid peroxidation and chlorophyll content in chickpea types colonized by different Glomus species under drought stress. Symbiosis 56(1), 5-18.
| Crossref | Google Scholar |
Tan ZL, Wang LF, Xiao XZ, Yang ZY (2008) Optimization of fermentation conditions and its applications to maize of Streptomyces microflavus 005. Soils and Fertilizers Sciences in China 2, 61-64.
| Google Scholar |
Tang D, Cheng P, Yang JJ, Li H, Sun JW, Wang K (2021) Physiological responses of plants to drought stress in the Northern Piedmont, Tianshan Mountains. Arid Zone Research 38(6), 1683-1694.
| Google Scholar |
Tian L, Liu JH, Zhao BP, Mi JZ, Li YH, Fei N (2020) Effects of combination of water-retaining agent and microbial fertilizer on dry matter accumulation, allocation, transportation and yield of oat in rainfed farmland. Chinese Journal of Ecology 39(9), 2996-3003.
| Google Scholar |
Tian F, Chen X, Wang PC, Zhong L, Ou E (2022) Effect of microbial agents on resistant enzyme system and biochemical indexes of drought resistance in Sophora davidii. Plant Physiology Journal 58(2), 435-446.
| Google Scholar |
Veen BW (1981) Relation between root respiration and root activity. Plant and Soil 63(1–2), 73-76.
| Crossref | Google Scholar |
Wang N, Yang Z, Ma XY, Wang H, Zhao Y, Yang T (2014) Effect of secondary metabolites of plant entophyte on physiological mechanism in pepper seedlings under drought stress. Northern Horticulture 22, 29-32.
| Google Scholar |
Wang HZ, Xu YL, Zhang CL, Han L (2015) Effects of drought stress on osmotic adjustment substances and antioxidant enzymes activity of Populus euphratica and Populus pruinosa seedlings. Journal of Arid Land Resources and Environment 29(12), 125-130.
| Google Scholar |
Wen HW, Yang B, Wang DS (2021) Research progress on promoting growth and drought resistance of wheat by plant growth promoting rhizobacteria. Journal of Nuclear Agricultural Science 35(9), 2194-2203.
| Google Scholar |
Xiaoli N, Hanmi Z, Xiukang W, Tiantian H, Puyu F, Ting L, Na Z, Dongxue Y (2020) Changes in root hydraulic conductance in relation to the overall growth response of maize seedlings to partial root-zone nitrogen application. Agricultural Water Management 229, 105839.
| Crossref | Google Scholar |
Xu Y, Zhang Z-M, Ding H, Qin F-F, Zhang G-C, Dai L-X (2022) Regulation of peanut seed germination and spermosphere microbial community structure by calcium fertilizer in acidic red soil. Acta Agronomica Sinica 48(8), 2088-2099.
| Crossref | Google Scholar |
Yang LY, Yang XL, Zhu MX, Yang YS, Wang CY (2020) Effects of drought stress on seed germination and seedling physiological characteristics of quinoa. Seed 39(9), 36-40.
| Google Scholar |
Yi B, Cui LJ, Song DX, Wang DX, Liu JG, Sun EY, Peng B, Li SL (2019) Effect of PEG simulated drought on biomass and root morphology of sunflower hybrids at seedling stage. Liaoning Agricultural Sciences 2, 8-14.
| Google Scholar |
Yıldırım K, Yağcı A, Sucu S, Tunç S (2018) Responses of grapevine rootstocks to drought through altered root system architecture and root transcriptomic regulations. Plant Physiology and Biochemistry 127, 256-268.
| Crossref | Google Scholar | PubMed |
Zhao Z, Chen W, Wang H, Xia KX, Gao RW, Jiang SQ, Pang G, Cai F (2018) Effects of bio-manure combined with chemical fertilizer reduced in application rate on soil fertility and yield and quality of tomato. Acta Pedologica Sinica 55(5), 1243-1253.
| Google Scholar |
Zhu SS, Mi JZ, Zhao BP, Sun MY, Li YH, Liu JH (2021) Effect of humic acid on carbon assimilation enzymes activity in leaves and oat yield under drought stress. Journal of Triticeae Crops 41(6), 722-730.
| Google Scholar |