Increasing agricultural losses due to biotic and abiotic stresses caused by climate change challenge food security worldwide. A promising strategy to sustain crop productivity under conditions of limited water availability is the use of plant growth promoting rhizobacteria (PGPR). Here, the effects of spore forming Bacillus licheniformis (FMCH001) on growth and physiology of maize (Zea mays L. cv. Ronaldinho) under well-watered and drought stressed conditions were investigated. Pot experiments were conducted in the automated high-throughput phenotyping platform PhenoLab and under greenhouse conditions. Results of the PhenoLab experiments showed that plants inoculated with B. licheniformis FMCH001 exhibited increased root dry weight (DW) and plant water use efficiency (WUE) compared to uninoculated plants. In greenhouse experiments, root and shoot DW significantly increased by more than 15% in inoculated plants compared to uninoculated control plants. Also, the WUE increased in FMCH001 plants up to 46% in both well-watered and drought stressed plants. Root and shoot activities of 11 carbohydrate and eight antioxidative enzymes were characterized in response to FMCH001 treatments. This showed a higher antioxidant activity of catalase (CAT) in roots of FMCH001 treated plants compared to uninoculated plants. The higher CAT activity was observed irrespective of the water regime. These findings show that seed coating with Gram positive spore forming B. licheniformis could be used as biostimulants for enhancing plant WUE under both normal and drought stress conditions.

Department of Adaptive Biotechnologies Global Change Research Institute Czech Academy of Sciences Brno Czechia

Department of Plant and Environmental Sciences Faculty of Science University of Copenhagen Taastrup Denmark

Plant Health Innovation Chr Hansen A S Hørsholm Denmark

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Akhtar S. S., Andersen M. N., Naveed M., Zahir Z. A., Liu F. (2015). Interactive effect of biochar and plant growth-promoting bacterial endophytes on ameliorating salinity stress in maize. Funct. Plant Biol. 42 770–781. PubMed

Albacete A., Cantero-Navarro E., Balibrea M. E., Großkinsky D. K., de la Cruz González M., Martínez-Andújar C., et al. (2014a). Hormonal and metabolic regulation of tomato fruit sink activity and yield under salinity. J. Exp. Bot. 65 6081–6095. 10.1093/jxb/eru347 PubMed DOI PMC

Albacete A., Cantero-Navarro E., Großkinsky D. K., Arias C. L., Balibrea M. E., Bru R., et al. (2014b). Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato. J. Exp. Bot. 66 863–878. 10.1093/jxb/eru448 PubMed DOI PMC

Belimov A. A., Dodd I. C., Safronova V. I., Shaposhnikov A. I., Azarova T. S., Makarova N. M., et al. (2015). Rhizobacteria that produce auxins and contain 1-amino-cyclopropane-1-carboxylic acid deaminase decrease amino acid concentrations in the rhizosphere and improve growth and yield of well-watered and water-limited potato (Solanum tuberosum). Ann. Appl. Biol. 167 11–25. 10.1111/aab.12203 DOI

Calvo-Polanco M., Sánchez-Romera B., Aroca R., Asins M. J., Declerck S., Dodd I. C., et al. (2016). Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environ. Exp. Bot. 131 47–57. 10.1016/j.envexpbot.2016.06.015 DOI

Cassán F., Vanderleyden J., Spaepen S. (2014). Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J. Plant Growth Regul. 33 440–459. 10.1007/s00344-013-9362-9364 DOI

Castillo P., Molina R., Andrade A., Vigliocco A., Alemano S., Cassán F. D. (2015). “Phytohormones and other plant growth regulators produced by PGPR: the genus Azospirillum,” in Handbook for Azospirillum: Technical Issues and Protocols, eds Cassán F. D., Okon Y., Creus C. M., (Cham: Springer International Publishing; ), 115–138. 10.1007/978-3-319-06542-7_7 DOI

Chakraborty U., Chakraborty B. N., Chakraborty A. P., Dey P. L. (2013). Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World J. Microbiol. Biotechnol. 29 789–803. 10.1007/s11274-012-1234-1238 PubMed DOI

Chen X. H., Koumoutsi A., Scholz R., Eisenreich A., Schneider K., Heinemeyer I., et al. (2007). Comparative analysis of the complete genome sequence of the plant growth–promoting bacterium Bacillus amyloliquefaciens FZB42. Nat. Biotechnol. 25 1007–1014. 10.1038/nbt1325 PubMed DOI

Chiappero J., Cappellari L. D. R., Sosa Alderete L. G., Palermo T. B., Banchio E. (2019). Plant growth promoting rhizobacteria improve the antioxidant status in Mentha piperita grown under drought stress leading to an enhancement of plant growth and total phenolic content. Ind. Crops Prod. 139:111553 10.1016/j.indcrop.2019.111553 DOI

Clements L. D., Miller B. S., Streips U. N. (2002). Comparative growth analysis of the facultative Anaerobes Bacillus subtilis, Bacillus licheniformis, and Escherichia coli. Syst. Appl. Microbiol. 25 284–286. 10.1078/0723-2020-2108 PubMed DOI

de Lima B. C., Moro A. L., Santos A. C. P., Bonifacio A., Araujo A. S. F., de Araujo F. F. (2019). Bacillus subtilis ameliorates water stress tolerance in maize and common bean. J. Plant Interact. 14 432–439. 10.1080/17429145.2019.1645896 DOI

Delaux P.-M., Radhakrishnan G. V., Jayaraman D., Cheema J., Malbreil M., Volkening J. D., et al. (2015). Algal ancestor of land plants was preadapted for symbiosis. Proc. Natl. Acad. Sci. U.S.A. 112:13390. 10.1073/pnas.1515426112 PubMed DOI PMC

Ehrlich P. R., Harte J. (2015). Opinion: to feed the world in 2050 will require a global revolution. Proc. Natl. Acad. Sci. U.S.A. 112:14743 10.1073/pnas.1519841112 PubMed DOI PMC

FAO and ITPS (2015). Status of the World’s Soil Resources (SWSR) – Technical Summary Food and Agriculture Organization of the United Nations and Intergovernmental Technical Panel on Soils. Rome: FAO.

Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S. M. A. (2009). Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29 185–212. 10.1051/agro:2008021 DOI

Fimognari L., Dölker R., Kaselyte G., Jensen C. N. G., Akhtar S. S., Großkinsky D. K., et al. (2020). Simple semi-high throughput determination of activity signatures of key antioxidant enzymes for physiological phenotyping. Plant Methods. 16:42 10.1186/s13007-020-00583-8 PubMed DOI PMC

Garcia-Lemos A. M., Gro kinsky D. K., Stokholm M. S., Lund O. S., Nicolaisen M. H., Roitsch T. G., et al. (2019). Root-associated microbial communities of abies nordmanniana: insights into interactions of microbial communities with antioxidative enzymes and plant growth. Front. Microbiol. 10:1937. 10.3389/fmicb.2019.01937 PubMed DOI PMC

Glick B. R. (2012). Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:963401 10.6064/2012/963401 PubMed DOI PMC

Glick B. R. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169 30–39. 10.1016/j.micres.2013.09.009 PubMed DOI

Glick B. R., Todorovic B., Czarny J., Cheng Z., Duan J., McConkey B. (2007). Promotion of plant growth by bacterial ACC deaminase. Crit. Rev. Plant Sci. 26 227–242. 10.1080/07352680701572966 DOI

Gowda V. R. P., Henry A., Yamauchi A., Shashidhar H. E., Serraj R. (2011). Root biology and genetic improvement for drought avoidance in rice. Field Crops Res. 122 1–13. 10.1016/j.fcr.2011.03.001 DOI

Großkinsky D. K., Svensgaard J., Christensen S., Roitsch T. (2015). Plant phenomics and the need for physiological phenotyping across scales to narrow the genotype-to-phenotype knowledge gap. J. Exp. Bot. 66 5429–5440. 10.1093/jxb/erv345 PubMed DOI

Großkinsky D. K., Syaifullah S. J., Roitsch T. (2018). Integration of multi-omics techniques and physiological phenotyping within a holistic phenomics approach to study senescence in model and crop plants. J. Exp. Bot. 69 825–844. 10.1093/jxb/erx333 PubMed DOI

Gururani M. A., Upadhyaya C. P., Baskar V., Venkatesh J., Nookaraju A., Park S. W. (2013). Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J. Plant Growth Regul. 32 245–258. 10.1007/s00344-012-9292-9296 DOI

Hendry G. A. F. (2008). Oxygen, free radical processes and seed longevity. Seed Sci. Res. 3 141–153. 10.1017/S0960258500001720 DOI

Honsdorf N., March T. J., Berger B., Tester M., Pillen K. (2014). High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines. PLoS One 9:e97047. 10.1371/journal.pone.0097047 PubMed DOI PMC

Hothorn T., Bretz F., Westfall P. (2008). Simultaneous inference in general parametric models. Biometrical J. 50 346–363. 10.1002/bimj.200810425 PubMed DOI

Jajic I., Sarna T., Strzalka K. (2015). Senescence, stress, and reactive oxygen species. Plants 4 393–411. 10.3390/plants4030393 PubMed DOI PMC

Jammer A., Gasperl A., Luschin-Ebengreuth N., Heyneke E., Chu H., Cantero-Navarro E., et al. (2015). Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. J. Exp. Bot. 66 5531–5542. 10.1093/jxb/erv228 PubMed DOI

Kasim W. A., Osman M. E., Omar M. N., Abd El-Daim I. A., Bejai S., Meijer J. (2013). Control of drought stress in wheat using plant-growth-promoting bacteria. J. Plant Growth Regul. 32 122–130. 10.1007/s00344-012-9283-9287 DOI

Kavar T., Maras M., Kidrič M., Šuštar-Vozlič J., Meglič V. (2008). Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol. Breed. 21 159–172. 10.1007/s11032-007-9116-9118 PubMed DOI

Khan N., Bano A., Zandi P. (2018). Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. J. Plant Interact. 13 239–247. 10.1080/17429145.2018.1471527 DOI

Kumar A., Verma J. P. (2018). Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol. Res. 207 41–52. 10.1016/j.micres.2017.11.004 PubMed DOI

Kumar S., Agarwal M., Dheeman S., Maheshwari D. K. (2015). “Exploitation of phytohormone-producing PGPR in development of multispecies bioinoculant formulation,” in Bacterial Metabolites in Sustainable Agroecosystem, ed. Maheshwari D. K., (Cham: Springer International Publishing; ), 297–317. 10.1007/978-3-319-24654-3_11 DOI

Kuska M. T., Behmann J., Großkinsky D. K., Roitsch T., Mahlein A.-K. (2018). Screening of barley resistance against powdery mildew by simultaneous high-throughput enzyme activity signature profiling and multispectral imaging. Front. Plant Sci. 9:1074. 10.3389/fpls.2018.01074 PubMed DOI PMC

Leser T. D., Knarreborg A., Worm J. (2008). Germination and outgrowth of Bacillus subtilis and Bacillus licheniformis spores in the gastrointestinal tract of pigs. J. Appl. Microbiol. 104 1025–1033. 10.1111/j.1365-2672.2007.03633.x PubMed DOI

Lim J.-H., Kim S.-D. (2013). Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol. J. 29 201–208. 10.5423/PPJ.SI.02.2013.0021 PubMed DOI PMC

Liu F., Jensen C. R., Shahanzari A., Andersen M. N., Jacobsen S.-E. (2005). ABA regulated stomatal control and photosynthetic water use efficiency of potato (Solanum tuberosum L.) during progressive soil drying. Plant Sci. 168 831–836. 10.1016/j.plantsci.2004.10.016 DOI

Lushchak V. I. (2014). Free radicals, reactive oxygen species, oxidative stress and its classification. Chem. Biol. Interact. 224 164–175. 10.1016/j.cbi.2014.10.016 PubMed DOI

Ma Y. (2019). Seed coating with beneficial microorganisms for precision agriculture. Biotechnol. Adv. 37:107423. 10.1016/j.biotechadv.2019.107423 PubMed DOI

Maheshwari D. K., Dheeman S., Agarwal M. (2015). “Phytohormone-producing PGPR for sustainable agriculture,” in Bacterial Metabolites in Sustainable Agroecosystem, ed. Maheshwari D. K., (Cham: Springer International Publishing; ), 159–182. 10.1007/978-3-319-24654-3_7 DOI

Nadeem S. M., Ahmad M., Zahir Z. A., Javaid A., Ashraf M. (2014). The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 32 429–448. 10.1016/j.biotechadv.2013.12.005 PubMed DOI

Nadeem S. M., Imran M., Naveed M., Khan M. Y., Ahmad M., Zahir Z. A., et al. (2017). Synergistic use of biochar, compost and plant growth-promoting rhizobacteria for enhancing cucumber growth under water deficit conditions. J. Sci. Food Agric. 97 5139–5145. 10.1002/jsfa.8393 PubMed DOI

Nair A. S., Abraham T. K., Jaya D. S. (2008). Studies on the changes in lipid peroxidation and antioxidants in drought stress induced cowpea (Vigna unguiculata L.) varieties. J. Environ. Biol. 29 689–691. PubMed

Naseem H., Bano A. (2014). Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J. Plant Interact. 9 689–701. 10.1080/17429145.2014.902125 DOI

Naveed M., Mitter B., Reichenauer T. G., Wieczorek K., Sessitsch A. (2014). Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ. Exp. Bot. 97 30–39. 10.1016/j.envexpbot.2013.09.014 DOI

Ngumbi E., Kloepper J. (2016). Bacterial-mediated drought tolerance: current and future prospects. Appl. Soil Ecol. 105 109–125. 10.1016/j.apsoil.2016.04.009 DOI

Nicholson W. L., Munakata N., Horneck G., Melosh H. J., Setlow P. (2000). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64 548–572. 10.1128/mmbr.64.3.548-572.2000 PubMed DOI PMC

Niu X., Song L., Xiao Y., Ge W. (2018). Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front. Microbiol. 8:2580. 10.3389/fmicb.2017.02580 PubMed DOI PMC

Noctor G., Mhamdi A., Foyer C. H. (2014). The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol. 164 1636–1648. 10.1104/pp.113.233478 PubMed DOI PMC

Pinheiro J., Bates D., DebRoy S., Sarkar D. R Core Team, (2019). nlme: Linear and Nonlinear Mixed Effects Models. Vienna: R Foundation for Statistical Computing.

R Core Team, (2017). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Radhakrishnan R., Hashem A., Abd Allah E. F. (2017). Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front. Physiol. 8:667. 10.3389/fphys.2017.00667 PubMed DOI PMC

Ryu C.-M., Farag M. A., Hu C.-H., Reddy M. S., Kloepper J. W., Paré P. W. (2004). Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134 1017–1026. 10.1104/pp.103.026583 PubMed DOI PMC

Saleem A. R., Bangash N., Mahmood T., Khalid A., Centritto M., Siddique M. T. (2015). Rhizobacteria capable of producing ACC deaminase promote growth of velvet bean (Mucuna pruriens) under water stress condition. Int. J Agric. Biol. 17 663–667. 10.17957/ijab/17.3.14.788 DOI

Setlow P. (1994). Mechanisms which contribute to the long-term survival of spores of Bacillus species. J. Appl. Bacteriol. 76 49S–60S. 10.1111/j.1365-2672.1994.tb04357.x PubMed DOI

Sgherri C. L. M., Maffei M., Navari-Izzo F. (2000). Antioxidative enzymes in wheat subjected to increasing water deficit and rewatering. J. Plant Physiol. 157 273–279. 10.1016/S0176-1617(00)80048-80046 DOI

Smart R. E., Bingham G. E. (1974). Rapid estimates of relative water content. Plant Physiol. 53 258–260. 10.1104/pp.53.2.258 PubMed DOI PMC

Tardieu F., Simonneau T., Muller B. (2018). The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annu. Rev. Plant Biol. 69 733–759. 10.1146/annurev-arplant-042817-40218 PubMed DOI

Turner N. C., Wright G. C., Siddique K. H. M. (2001). Adaptation of grain legumes (pulses) to water-limited environments. Adv. Agron. 71 193–231. 10.1016/s0065-2113(01)71015-2 DOI

Vejan P., Abdullah R., Khadiran T., Ismail S., Nasrulhaq Boyce A. (2016). Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Molecules 21:E573. 10.3390/molecules21050573 PubMed DOI PMC

Vurukonda S. S. K. P., Vardharajula S., Shrivastava M., SkZ A. (2016). Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 184 13–24. 10.1016/j.micres.2015.12.003 PubMed DOI

Xu M., Sheng J., Chen L., Men Y., Gan L., Guo S., et al. (2014). Bacterial community compositions of tomato (Lycopersicum esculentum Mill.) seeds and plant growth promoting activity of ACC deaminase producing Bacillus subtilis (HYT-12-1) on tomato seedlings. World J. Microbiol. Biotechnol. 30 835–845. 10.1007/s11274-013-1486-y PubMed DOI

Zheng W., Zeng S., Bais H., LaManna J. M., Hussey D. S., Jacobson D. L., et al. (2018). Plant growth-promoting rhizobacteria (PGPR) reduce evaporation and increase soil water retention. Water Resour. Res. 54 3673–3687. 10.1029/2018wr022656 DOI

Zhou C., Zhu L., Xie Y., Li F., Xiao X., Ma Z., et al. (2017). Bacillus licheniformis SA03 confers increased saline-alkaline tolerance in chrysanthemum plants by induction of abscisic acid accumulation. Front. Plant Sci. 8:1143. 10.3389/fpls.2017.01143 PubMed DOI PMC

Antioxidant Responses and Redox Regulation Within Plant-Beneficial Microbe Interaction

Stimulation of Arabidopsis thaliana Seed Germination at Suboptimal Temperatures through Biopriming with Biofilm-Forming PGPR Pseudomonas putida KT2440

Presence and future of plant phenotyping approaches in biostimulant research and development

Integration of Phenomics and Metabolomics Datasets Reveals Different Mode of Action of Biostimulants Based on Protein Hydrolysates in Lactuca sativa L. and Solanum lycopersicum L. Under Salinity

Identification of Root-Associated Bacteria That Influence Plant Physiology, Increase Seed Germination, or Promote Growth of the Christmas Tree Species Abies nordmanniana

Burkholderia Phytofirmans PsJN Stimulate Growth and Yield of Quinoa under Salinity Stress