Polyamine-producing actinobacteria enhance biomass production and seed yield in Salicornia bigelovii

Acuna JJ, Campos M, Mora ML, Jaisi DP, Jorquera MA (2019) ACCD-producing rhizobacteria from an Andean Altiplano native plant (Parastrephia quadrangularis) and their potential to alleviate salt stress in wheat seedlings. Appl Soil Ecol 136:184–190

Ahmad JS, Baker R (1987) Rhizosphere competence of Trichoderma harzianum. Phytopathology 77:182–189

Al-Yamani W, Kennedy S, Sgouridis S, Yousef L (2013) A hand suitability study for the sustainable cultivation of the halophyte Salicornia bigelovii: the case of Abu Dhabi, UAE. Arid Land Res Manag 27:349–360

Anwar S, Ali B, Sajid I (2016) Screening of rhizospheric actinomycetes for various in-vitro and in-vivo plant growth promoting (PGP) traits and for agroactive compounds. Front Microbiol 7:1334

Arena ME, Manca de Nadra MC (2001) Biogenic amine production by Lactobacillus. J Appl Microbiol 90:158–162

Bashan Y, Puente ME, Myrold DD, Toledo G (1998) In vitro transfer of fixed nitrogen from diazotrophic filamentous cyanobacteria to black mangrove seedlings. FEMS Microbiol Ecol 26:165–170

Bashan Y, Moreno M, Troyo E (2000) Growth promotion of the seawater-irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp. Biol Fertil Soils 32:265–272

Bashan Y, Kamnev AA, de-Bashan LE (2013) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479

Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998-2013). Plant Soil 378:1–33

Ben Abdallah D, Frikha-Gargouri O, Tounsi S (2018) Rizhospheric competence, plant growth promotion and biocontrol efficacy of Bacillus amyloliquefaciens subsp. plantarum strain 32a. Biol Control 124:61–67

Benizri E, Baudoin E, Guckert A (2001) Root colonization by inoculated plant growth-promoting rhizobacteria. Biocontrol Sci Tech 11:557–574

Beranger-Novat N, Monin J, Martin-Tanguy J (1994) Polyamines and their biosynthetic enzymes in dormant embryos of the spindle tree (Euonymus europaeus L.) and in dormancy break obtained after treatment with gibberellic acid. Plant Sci 102:139–145

Besford RT, Richardson CM, Campos JL, Tiburcio AF (1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189:201–206

Biswas K, Choudhury JD, Mahansaria R, Saha M, Mukherjee J (2017) Streptomyces euryhalinus sp. nov., a new actinomycete isolated from a mangrove forest. J Antibiot 70:747–753

Blair GJ, Chinoim N, Lefroy RDB, Anderson GC, Crocker GJ (1991) A soil sulfur test for pastures and crops. Aust J Soil Res 29:619–626

Bueno M, Cordovilla M-P (2019) Polyamines in halophytes. Front Plant Sci 10:439

Cai Q, Zhang J, Guo C, Al E (2006) Reviews of the physiological roles and molecular biology of polyamines in higher plants. J Fujian Educ Coll 7:118–124

Capper AL, Higgins KP (1993) Application of Pseudomonas fluorescens isolates to wheat as potential biological control agents against take-all. Plant Pathol 42:560–567

Cassán F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19

Chanway CP, Nelson LM, Holl FB (1988) Cultivar-specific growth promotion of spring wheat (Triticum aestivum L.) by coexistent Bacillus species. Can J Microbiol 34:925–929

Chanway CP, Radley RA, Holl FB (1991) Inoculation of conifer seed with plant growth promoting Bacillus strains causes increased seedling emergence and biomass. Soil Biol Biochem 23:575–580

Chaurasia A, Meena BR, Tripathi AN, Pandey KK, Rai AB, Singh B (2018) Actinomycetes: an unexplored microorganisms for plant growth promotion and biocontrol in vegetable crops. World J Microbiol Biotechnol 34:132

Chen D, Shao Q, Yin L, Younis A, Zheng B (2018) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945

Colwell JD (1965) An automatic procedure for the determination of phosphorus in sodium hydrogen carbonate extracts of soils. Chem Ind 22:893–895

Cross T (1989) Growth and examination of actinomycete, some guidelines. In: Williams ST, Sharpe ME, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 4. Williams and Wilkins, Baltimore, pp 2340–2343

Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

Davies BH (1965) Analysis of carotenoid pigments. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments. Academic Press, London, pp 489–532

di Menna ME (1957) The isolation of yeasts from soil. J Gen Microbiol 17:678–688

Diao Q, Song Y, Shi D, Qi H (2017) Interaction of polyamines, abscisic acid, nitric oxide, and hydrogen peroxide under chilling stress in tomato (Lycopersicon esculentum Mill.) seedlings. Front Plant Sci 8:203

Doncato KB, Costa CSB (2018) Nutritional potential of a novel sea asparagus, Salicornia neei Lag., for human and animal diets. Biotemas 31:57–63

Dworkin M, Foster J (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–601

Dye DW (1962) The inadequacy of the usual determinative tests for identification of Xanthomonas spp. NZT Sci 5:393–416

El-Tarabily KA (2008) Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere-competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycete actinomycetes. Plant Soil 308:161–174

El-Tarabily KA, AlKhajeh AS, Ayyash MM, Alnuaimi LH, Sham A, ElBaghdady KZ, Tariq S, AbuQamar SF (2019) Growth promotion of Salicornia bigelovii by Micromonospora chalcea UAE1, an endophytic 1-aminocyclopropane-1-carboxylic acid deaminase-producing actinobacterial isolate. Front Microbiol 10:1694

Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706

Glenn EP, Brown JJ, O'Leary JW (1998) Irrigating crops with seawater. Sci Am 279:76–81

Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

Goodfellow M, Williams S (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216

Grover M, Bodhankar S, Maheswari M, Srinivasarao C (2016) Actinomycetes as mitigators of climate change and abiotic stress. In: Subramaniam G, Arumugam S, Rajendran V (eds) Plant growth promoting actinobacteria. A new avenue for enhancing the productivity and soil fertility of grain legumes. Springer, New York, pp 203–212

Guinn G, Brummett DL, Beier RC (1986) Purification and measurement of abscisic acid and indole-acetic acid by high performance liquid chromatography. Plant Physiol 81:997–1002

Holden M (1965) Chlorophylls. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments. Academic Press, London, pp 462–488

Holguin G, Guzman MA, Bashan Y (1992) Two new nitrogen-fixing bacteria from the rhizosphere of mangrove trees: their isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp. FEMS Microbiol Ecol 101:207–216

Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soils 33:265–278

Jha B, Gontia I, Hartmann A (2012) The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 356:265–277

Jiménez-Bremont JF, Marina M, Guerrero-González ML, Rossi FR, Sánchez-Rangel D, Rodríguez-Kessler M, Ruiz OA, Gárriz A (2014) Physiological and molecular implications of plant polyamine metabolism during biotic interactions. Front Plant Sci 5:95

Jizhong X, Haijiang C, Baokun M, Wencai Z (2001) Effects of exogenous spermidine on the levels of endogenous hormones and polyamines in the flowers and fruitlets of red Fuji apple. Acta Horticulturae Sinica 28:206–210

Kadereit G, Ball P, Beer S, Mucina L, Sokoloff D, Teege P, Yaprak AE, Freitag H (2007) A taxonomic nightmare comes true: phylogeny and biogeography of glassworts (Salicornia L., Chenopodiaceae). Taxon 56:1143–1170

Kakkar R, Rai V, Nagar P (1997) Polyamine uptake and translocation in plants. Biol Plantarum 40:481–491

Kämpfer P (2012) Genus I. Streptomyces. Waksman and Henrici 1943, 339AL emend. Witt and Stackebrandt 1990, 370 emend. Wellington, Stackebrandt, Sanders, Wolstrup and Jorgensen 1992, 159. In: Whitman W, Goodfellow M, Kämpfer P, Busse H-J, Trujillo M, Ludwig W, Suzuki K (eds) Bergey’s manual of systematic bacteriology, vol 5, 2nd. Part B edn. Springer, New York, pp 1455–1767

Kortemaa H, Rita H, Haahtela K, Smolander A (1994) Root colonization ability of antagonistic Streptomyces griseoviridis. Plant Soil 163:77–83

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

Kumar A, Patel JS, Meena VS, Ramteke PW (2019) Plant growth-promoting rhizobacteria: strategies to improve abiotic stresses under sustainable agriculture. J Plant Nutr 42:1402–1415

Küster E (1959) Outline of a comparative study of criteria used in characterization of the actinomycetes. Int Bull Bact Nomen Taxon 9:97–104

Liu J, Nada K, Pang X, Honda C, Kitashiba H, Moriguchi T (2006) Role of polyamines in peach fruit development and storage. Tree Physiol 26:791–798

Loconsole D, Cristiano G, De Lucia B (2019) Glassworts: from wild salt marsh species to sustainable edible crops. Agriculture 9:14

Machàckovà I, Krekule J, Eder J, Seidlovà F, Strnad M (1993) Cytokinins in photoperiodic induction of flowering Chenopodium species. Physiol Plantarum 87:160–166

Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D, Borin S (2013) Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. Biomed Res Int 2013:248078

Marchetti CF, Ugena L, Humplík JF, Polák M, Ćavar Zeljković S, Podlešáková K, Fürst T, De Diego N, Spíchal L (2019) A novel image-based screening method to study water-deficit response and recovery of barley populations using canopy dynamics phenotyping and simple metabolite profiling. Front Plant Sci 10:1252

Marino M, Maifreni M, Moret S, Rondinini G (2000) The capacity of Enterobacteriaceae species to produce biogenic amines in cheese. Lett Appl Microbiol 31:169–173

Mathew BT, Torky Y, Amin A, Mourad A-HI , Ayyash MM, El Keblawy A, AbuQamar SF, El-Tarabily KA (2020) Halophilic marine actinobacteria isolated from the rhizosphere of Salicornia bigelovii promote its growth and seed production using seawater irrigation. Front Microbiol 11:552

Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175

Misaghi IJ, Donndelinger IJ (1990) Endophytic bacteria in symptom-free cotton plants. Phytopathology 80:808–811

Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

Mustafavi SH, Badi HN, Sekara A, Al E (2018) Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiol Plant 40:102

Nag S, Saha K, Choudhuri MA (2001) Role of auxins and polyamines in adventitious root formation in relation to changes in compounds involved in rotting. J Plant Growth Regul 20:182–194

Nambeesan S, AbuQamar S, Laluk K, Mattoo AK, Mickelbart MV, Ferruzzi MG, Mengsite T, Handa AK (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol 158:1034–1045

Nassar AH, El-Tarabily KA, Sivasithamparam K (2003) Growth promotion of bean (Phaseolus vulgaris L.) by a polyamine-producing isolate of Streptomyces griseoluteus. Plant Growth Regul 40:97–106

Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

Nonomura H, Hayakawa M (1988) New methods for the selective isolation of soil actinomycetes. In: Okami Y, Beppu T, Oegawara H (eds) Biology of actinomycetes. Japan Science Society Press, Tokyo, pp 288–293

Ohshima T (2007) Unique polyamines produced by an extreme thermophile, Thermus thermophilus. Amino Acids 33:367–372

Olanrewaju OS, Babalola OO (2019) Streptomyces: implications and interactions in plant growth promotion. Appl Microbiol Biotechnol 103:1179–1188

Parenti F, Pagani H, Beretta G (1975) Lipiarmycin, a new antibiotic from Actinoplanes. I Description of the producer strain and fermentation studies. J Antibiot 28:247–252

Parvin S, Lee OR, Sathiyaraj G, Al E (2014) Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system. Gene 537:70–78

Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370

Podlešáková K, Ugena L, Spíchal L, Doležal K, De Diego N (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 48:53–65

Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092

Rayment GE, Higginson FR (1992) Australian laboratory handbook of soil and water chemical methods. Inkata Press, Melbourne, p 330

Redmond JW, Tseng A (1979) High-pressure liquid chromatographic determination of putrescine, spermidine and spermine. J Chromatogr 170:479–481

Rojas A, Holguin G, Glick BR, Bashan Y (2001) Synergism between Phyllobacterium sp. (N2-fixer) and Bacillus licheniformis (P-solubilizer), both from a semiarid mangrove rhizosphere. FEMS Microbiol Ecol 35:181–187

Rueda-Puente EO, Castellanos T, Troyo-Diéguez E, León-Alvarez JL (2004) Effect of Klebsiella pneumoniae and Azospirillum halopraeferens on the growth and development of two Salicornia bigelovii genotypes. Aust J Exp Agr 44:65–74

Schreiter S, Babin D, Smalla K, Grosch R (2018) Rhizosphere competence and biocontrol effect of Pseudomonas sp. RU47 independent from plant species and soil type at the field scale. Front Microbiol 9:97

Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

Searle PL (1984) The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. A review. Analyst 109:549–568

Sham A, Al-Ashram H, Whitley K, Iratni R, El-Tarabily K, AbuQamar S (2019) Metatranscriptomic analysis of multiple environmental stresses identifies RAP2.4 gene associated with Arabidopsis immunity to Botrytis cinerea. Sci Rep 9:17010

Shepherd KA, MacFarlane TD, Colmer TD (2005) Morphology, anatomy and histochemistry of Salicornioideae (Chenopodiaceae) fruits and seeds. Ann Bot 95:917–933

Shindy WW, Smith OE (1975) Identification of plant hormones from cotton ovules. Plant Physiol 55:550–554

Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

Smith MA, Davies PJ (1985) Separation and quantitation of polyamines in plant tissue by high performance liquid chromatography of their dansyl derivatives. Plant Physiol 78:89–91

Strzelczyk E, Pokojska-Burdziej A (1984) Production of auxins and gibberellin-like substances by mycorrhizal fungi, bacteria and actinomycetes isolated from the soil and the mycorrhizosphere of pine (Pinus silvestris L.). Plant Soil 81:185–194

Tamm O (1922) Determination of the inorganic components of the gel-complex in soils. Medd Stat Skogförsöd 19:387–404

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

Tien TM, Gaskings MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37:1016–1024

Todorov D, Alexieva V, Karanov E (1998) Effect of putrescine, 4-PU-30, and abscisic acid on maize plants grown under normal, drought and rewatering conditions. J Plant Growth Regul 17:197–203

Ugena L, Hýlová A, Podlešáková K, Humplík JF, Doležal K, Diego N, Spíchal L (2018) Characterization of biostimulant mode of action using novel multi-trait high-throughput screening of Arabidopsis germination and rosette growth. Front Plant Sci 9:1327

Upreti KK, Murti GGR (1999) Effect of polyamines on the changes in endogenous hormones in pea under water stress conditions. Indian J Plant Physiol 4:1–5

Walkely A, Black LA (1934) An examination of the Degjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

Weller DM (1988) Biological control of soil-borne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407

Wellington EMH, Williams ST (1977) Preservation of actinomycete inoculum in frozen glycerol. Microbios Lett 6:151–157

Williams ST, Shameemullah M, Watson ET, Mayfield CI (1972) Studies on the ecology of actinomycetes in soil. VI. The influence of moisture tension on growth and survival. Soil Biol Biochem 4:215–225

Wu J, Shu S, Li C, Sun J, Guo S (2018) Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. Plant Physiol Biochem 128:152–162

Xu L, Xing ST, Sun X (2014) Effects of polyamines on hormones contents and the relationship with the flower bud differentiation in chrysanthemum. Plant Physiol J 50:1195–1202

Zheleva D, Tsonev T, Sergiev I, Karanov E (1994) Protective effect of exogenous polyamines against atrazine in pea plants. J Plant Growh Regul 13:203–211

Zhou C, Ma Z, Zhu L, Xiao X, Xie Y, Zhu J, Wang J (2016) Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int J Mol Sci 17:976