Physiological response of North China red elder container seedlings to inoculation with plant growth-promoting rhizobacteria under drought stress

Autoři: FangChun Liu aff001;  HaiLin Ma aff001;  ZhenYu Du aff001;  BingYao Ma aff001;  XingHong Liu aff001;  Lin Peng aff001;  WenXin Zhang aff001
Působiště autorů: Institute of Resource and Environment, Shandong Academy of Forestry, Jinan, Shandong, China aff001;  Shandong Engineering Research Center for Ecological Restoration of Forest Vegetation, Jinan, Shandong, China aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226624


The issue of how to alleviate the negative effects imposed by water stress is an interesting problem. Plant growth-promoting rhizobacteria (PGPR) colonize the rhizosphere of plants and are known to promote the growth of crops. However, there are few studies characterizing the physiological response of plants to drought stress after PGPR inoculation. The aim of this study was to investigate the effectiveness of different PGPRs in arid environments and then investigated the effects of PGPR inoculation under drought stress on the physiological characteristics and growth of North China red elder (Sambucus williamsii) nursery container seedlings. The viable count of different PGPRs under drought stress varies widely, and the drought tolerance of Acinetobacter calcoaceticus X128 was significantly higher than that of other PGPRs. In comparison with non-inoculation, inoculation with X128 in an arid environment significantly increased stomatal conductance and mitigated the inhibition of net photosynthetic rate caused by drought stress; this mitigating effect of inoculation is enhanced as the level of drought stress increases. Relative to non-inoculated seedlings, cytokinin levels in the leaves increased by 91.17% under severe drought stress conditions in inoculated seedlings. However, X128 inoculation decreased this deficit to only 44.54%. Compared with non-inoculated seedlings, the relative water content of inoculated seedlings under severe drought stress increased by 15.06%, however the relative conductivity decreased by 12.48%. Consequently, X128 could increase dry matter accumulation of S. williamsii regardless of watering status, indicative of the greater benefits of PGPR on shoot growth than root. Therefore, inoculation of A. calcoaceticus X128 under drought conditions play a significant role for alleviating the negative effects imposed by water stress and promoting plant growth.

Klíčová slova:

Cytokinins – Drought adaptation – Leaves – Plant physiology – Plant resistance to abiotic stress – Seedlings – Stomata – Water resources


1. Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res. 2016; 184:13–24. doi: 10.1016/j.micres.2015.12.003 26856449

2. Kavamuraa VN, Santosa SN, Silva JL, Parmaa MM, Ávilaa LA, Viscontia A, Zucchia TD, Taketania RG, Andreoteb FD, Meloa IS. Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol Res. 2013; 168:183–191 doi: 10.1016/j.micres.2012.12.002 23279812

3. Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol. 2005; 16:123–132 doi: 10.1016/j.copbio.2005.02.001 15831376

4. Kasim WA, Osman ME, Omar MN, El-Daim IAA, Bejai S, Meijer J. Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul. 2013; 32:122–130

5. Ali F, Bano A, Fazal A. Recent methods of drought stress tolerance in plants. Plant Growth Regul. 2017; 82:363–375

6. Soussi A, Ferjani R, Marasco R, Guesmi A, Cherif H, Rolli E, Mapelli F, Ouzari HI, Daffonchio D, Cherif A. Plant-associated microbiomes in arid lands: diversity, ecology and biotechnological potential. Plant Soil. 2016; 405:357–370

7. Bartlett MK, Klein T, Jansen S, Choat B, Sack L. The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc Natl Acad Sci U S A. 2016; 113:13098–13103 doi: 10.1073/pnas.1604088113 27807136

8. Bellasio C, Quirk J, Beerling D J. Stomatal and non-stomatal limitations in savanna trees and C4 grasses grown at low, ambient and high atmospheric CO2. Plant Science. 2018; 274:181–192 doi: 10.1016/j.plantsci.2018.05.028 30080602

9. Seki M Umezawa T, Urano K, Shinozaki K. Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol. 2007; 10:296–302 doi: 10.1016/j.pbi.2007.04.014 17468040

10. Ribas-Carbo M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J. Effects of water stress on respiration in soybean leaves. Plant Physiol. 2005; 139:466–473 doi: 10.1104/pp.105.065565 16126857

11. Mouillon JM, Gustafsson P, Harryson P. Structural investigation of disordered stress proteins comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiol. 2006; 141:638–650 doi: 10.1104/pp.106.079848 16565295

12. Niu X, Song L, Xiao Y, Ge W. Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front. 2019; doi: 10.3389/fmicb.2017.02580 29379471

13. Prudent M, Salon C, Souleimanov A, Neil Emery RJ, Smith DL. Soybean is less impacted by water stress using Bradyrhizobium japonicum and thuricin-17 from Bacillus thuringiensis. Agron Sustain Dev. 2015; 35:749–757

14. Cohena AC, Bottinia R, Pontina M, Berlia FJ, Morenoa D, Boccanlandroa H, Travagliac CN, Piccolia PN. Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant. 2015; 153:79–90 doi: 10.1111/ppl.12221 24796562

15. Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M. Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol. 2011; 27:197–205

16. Rubin RL, Groenigen KJV, Hungate BA. Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis. Plant Soil. 2017; 416:309–323

17. Abbasi MK, Sharif S, Kazmi M, Sultan T, Aslam M. Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants. Plant Biosyst. 2011; 145:159–168

18. Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR. Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil. 2005; 272:201–209

19. Krey T, Caus M, Baum C, Ruppel S, Eichler-Löbermann B. Interactive effects of plant growth–promoting rhizobacteria and organic fertilization on P nutrition of Zea mays L. and Brassica napus L. J Plant Nutr Soil Sci. 2011; 174:602–613

20. Liu D, Yang Q, Ge K, Qi G, Du B, Ding Y. Promotion of iron nutrition and growth on peanut by Paenibacillus illinoisensis and Bacillus sp. Strains. Braz J Microbiol. 2017; 48:656–670 doi: 10.1016/j.bjm.2017.02.006 28645648

21. Vessey JK. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil. 2003; 255:571–586

22. Yang J, Kloepper JW, Ryu CM. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 2009; 14:1–4 doi: 10.1016/j.tplants.2008.10.004 19056309

23. Liu F, Xing S, Ma H, Du Z, Ma B. Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol. 2013; 97:9155–9164 doi: 10.1007/s00253-013-5193-2 23982328

24. Rubin RL, Groenigen KJ, Hungate BA. Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis. Plant Soil; 2017:416:309–323.

25. Timmusk S, Wagner EGH. The plant growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene ssion: a possible connection between biotic and abiotic stress responses. Mol Plant-Microb Interact. 1999; 12:951–959

26. Mayaka S, Tirosh T, Glick B R. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 2004; 166:525–530

27. Šmehilová M, Dobrůšková J, Novák O, Takáč T, Galuszka P. Cytokinin-specific glycosyltransferases possess different roles in cytokinin homeostasis maintenance. Front Plant Sci. 2016; doi: 10.3389/fpls.2016.01264 27602043

28. Wang S, Wang S, Sun Q, Yang L, Zhu Y, Yuan Y, Hua J. A Role of Cytokinin Transporter in Arabidopsis Immunity. Molecular Plant-Microbe Interactions. 2017; 30:325–333 doi: 10.1094/MPMI-01-17-0011-R 28398838

29. Weyens N, Lelie DVD, Taghavi S, Newman L, Vangronsveld J. Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 2009; 27:591–598 doi: 10.1016/j.tibtech.2009.07.006 19683353

30. Yang B, Lin X, Yang C, Tan J, Li W, Kuang H. Sambucus Williamsii Hance promotes MC3T3-E1 cells proliferation and differentiation via BMP-2/Smad/p38/JNK/Runx2 signaling pathway. Phytother Res. 2015; 29:1692–1699 doi: 10.1002/ptr.5482 26455827

31. Yang B, Lin X, Tan J, She X, Liu Y, Kuang H. Root bark of Sambucus Williamsii Hance promotes rat femoral fracture healing by the BMP-2/Runx2 signaling pathway. J Ethnopharmacol. 2016; 191: 107–114 doi: 10.1016/j.jep.2016.05.017 27178636

32. South DB, Harris SW, Barnett JP, Hainds MJ, Gjerstad DH. Effect of container type and seedling size on survival and early height growth of Pinus palustris seedlings in Alabama, U.S.A. For Ecol Manag. 2005; 204:385–398

33. Liu FC, Xing SJ, Ma HL, Du ZY, Ma BY. Plant growth-promoting rhizobacteria affect the growth and nutrient uptake of Fraxinus americana container seedlings. Appl Microbiol Biotechnol. 2013; 97:4617–4625 doi: 10.1007/s00253-012-4255-1 22777281

34. Hou X, Yu X, Du B, Liu K, Yao L, Zhang S, Selin C, Fernando WGD, Wang C, Ding Y. A single amino acid mutation in Spo0A results in sporulation deficiency of Paenibacillus polymyxa SC2. Res Microbiol. 2016; 167:472–479 doi: 10.1016/j.resmic.2016.05.002 27208661

35. Hussain A, Hasnain S. Phytostimulation and biofertilization in wheat by cyanobacteria. J Ind Microbiol Biotechnol 2010; 38:85–92 doi: 10.1007/s10295-010-0833-3 20820860

36. Barrs HD, Weatherley PE. A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci. 1962; 15:413–428

37. Sheik CS, Beasley WH, Elshahed MS, Zhou X, Luo Y, Krumholz LR. Effect of warming and drought on grassland microbial communities. The ISME Journal. 2011; 5:1692–1700 doi: 10.1038/ismej.2011.32 21451582

38. Pereyra MA, Ballesteros FM, Creus CM, Creus CM, Sueldo RJ, Barass CA. Seedlings growth promotion by Azospirillum brasilense under normal and drought conditions remains unaltered in Tebuconazole-treated wheat seeds. Europ J Soil Biol. 2009; 45:20–27

39. Guerfel M, Baccouri O, Boujnah D, Chaibi W, Zarrouk M. Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. Sci Hortic. 2009; 119:257–263

40. Verma J P, Yadav J, Tiwari KN, Lavakush, Singh V. Impact of plant growth promoting rhizobacteria on crop production. Int J Agric Res. 2010; 5:954–983

41. Wu FZ, Bao WK, Li FL, Wu N. Effects of water stress and nitrogen supply on leaf gas exchange and fluorescence parameters of Sophora davidii seedlings. Photosynthetica. 2008; 46:40–48

42. Vysotskaya L B, Kudoyarova GR, Veselov SU, Jones HG. Unusual stomatal behaviour on partial root excision in wheat seedlings. Plant Cell Environ, 2003; 27:69–77

43. Merewitz EB, Du H, Yu W, Liu Y, Gianfagna T, Huang B. Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot. 2012; 63:1315–1328 doi: 10.1093/jxb/err372 22131157

44. Arkhipova TN, Prinsen E, Veselov SU. Martinenko EV, Melentiev AI. Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil. 2007; 292: 305–315

45. Davies WJ, Kudoyarova G, Hartung W. Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. Journal of Plant Growth Regul. 2005; 24:285–295

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