Abstract
Titanium ions significantly promote plant growth, but the mechanism is still unclear. Cut flowers are ideal materials for the study of plant growth and senescence. In this study, freshly cut Gerbera jamesonii were used to study the effects of titanium ions (8 mg/L) on the flower longevity. Flowering observation showed that the gerbera vase life was significantly prolonged in the presence of titanium ions. Plate colony counts showed that the amounts of bacteria in the vase solution of the control group were approximately 1700 times more than that of titanium ion treatment group. High-throughput sequencing was used to determine the sequences of 16S rRNA gene V3-V4 variable regions of the vase solutions to analyze bacterial species, their average proportions, and absolute abundance. The results showed that the titanium ions reduced the entire bacterial counts as well as altered the absolute abundance of different bacterial species in the vase solution. The most prevalent bacteria were mainly Enterobacteriaceae, Pseudomonas veronii, Pseudomonas sp., Delftia sp., Agrobacterium sp., Sphingobacterium multivorum, Acinetobacter johnsonii, and Clostridiaceae. In combination with plate colony counts, we demonstrated that all the bacterial growths were significantly inhibited by titanium ions, regardless of their average proportions increased or decreased. These results showed that titanium ions could extend effectively the longevity of gerberas and possess the broad-spectrum antibacterial properties. This study provides a basis for further mechanism exploration of titanium ions action and its applications in cut flower preservation and agricultural production.
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17 August 2020
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References
Danaee E, Mostofi Y, Moradi P (2011) Effect of GA3 and BA on postharvest quality and vase life of gerbera (Gerbera jamesonii. cv. Good Timing) cut flowers. Hortic Environ Biotechnol 52:140–144
Osbel MF, Maritza E, Teixeira da Silva J, Danilo TPM, Marcos ADG (2017) In vitro propagation of Gerbera jamesonii Bolus ex Hooker f. in a temporary immersion bioreactor. Plant Cell Tissue Organ Cult 129:543–551
Macnish AJ, Leonard RT, Nell TA (2008) Treatment with chlorine dioxide extends the vase life of selected cut flowers. Postharvest Biol Technol 50:197–207
Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83
Goszczyńska D, Rudnicki RM (1982) Long-term storage of carnations cut at the green-bud stage. Sci Hortic 17(3):289–297
Ketsa S, Piyasaengthong Y, Prathuangwong S (1995) Mode of action of AgNO3 in maximizing vase life of Dendrobium 'Pompadour' flowers. Postharvest Biol Technol 5:109–117
Veen H (1979) Effects of silver on ethylene synthesis and action in cut carnations. Planta 145:467–470
Ichimura K, Hiraya T (1999) Effect of silver thiosulfate complex (STS) in combination with sucrose on the vase life of cut sweet pea [Lathyrus odoratus] flowers. J Jpn Soc Hortic Sci 68:23–27
Pun Um K (2003) Role of sugars in senescence and biosynthesis of ethylene in cut flowers. Jpn Agr Res Q 37:219–224
Barksdale J (1950) Titanium, its occurrence, chemistry, and technology. Soil Sci 70:414
Noort RV (1987) Titanium: the implant material of today. J Mater Sci 22:3801–3811
Haghighi M, Heidarian S, Teixeira da Silva JA (2012) The effect of titanium amendment in N-withholding nutrient solution on physiological and photosynthesis attributes and micronutrient uptake of tomato. Biol Trace Elem Res 150:381–390
Cígler P (2002) Contribution to understanding the mechanism of titanium action in plant. J Plant Nutr 25:577–598
Yaghoubi S, Schwietert CW, Mccue JP (2000) Biological roles of titanium. Biol Trace Elem Res 78:205–217
Klamkowski K (2005) “Szampion” apple tree response to foliar titanium application. J Plant Nutr 27:2033–2046
Raliya R, Nair R, Chavalmane S, Wang W-N, Biswas P (2015) Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant. Metallomics 7:1584–1594
Suwalsky M, Villena F, Norris B, Soto MA, Sotomayor CP, Messori L, Zatta P (2005) Structural effects of titanium citrate on the human erythrocyte membrane. J Inorg Biochem 99:764–770
Collins JM, Uppal R, Incarvito CD, Valentine AM (2005) Titanium(IV) citrate speciation and structure under environmentally and biologically relevant conditions. Inorg Chem 44:3431–3440
Kuchmii SY, Korzhak AV, Kryukov AI (1985) Photolysis of titanium (III) complexes in alcoholic matrices at 77 K. Theor Exp Chem 21:458–461
Harrigan RW, Hammond GS, Gray HB (1974) Photochemistry of titanocene (IV) derivatives. J Organomet Chem 81:79–85
Paradies J, Crudass J, MacKay F, Yellowlees LJ, Montgomery J, Parsons S, Oswald I, Robertson N, Sadler PJ (2006) Photogeneration of titanium(III) from titanium(IV) citrate in aqueous solution. J Inorg Biochem 100(7):1260–1264
Ju F, Zhang T (2015) 16S rRNA gene high-throughput sequencing data mining of microbial diversity and interactions. Appl Microbiol Biotechnol 99:4119–4129
Cleary DFR, de VNJ, Polónia ARM, Freitas R, Gomes NCM (2015) Composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in the Spermonde Archipelago, Indonesia. Microb Ecol 70:889–903
LaMontagne MG, Schimel JP, Holden PA (2003) Comparison of subsurface and surface soil bacterial communities in California grassland as assessed by terminal restriction fragment length polymorphisms of PCR-amplified 16S rRNA genes. Microb Ecol 46(2):216–227
Maclean D, Jones JD, Studholme DJ (2009) Application of 'next-generation' sequencing technologies to microbial genetics. Nat Rev Microbiol 7:287–296
Hong C, Si Y, Xing Y, Li Y (2015) Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ Sci Pollut Res Int 22:10788–10799
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Fan YF, Wei CM, Li CX, Wang L, Li XY, Ma XR (2016) Antimicrobial activity of titanium ion of variable valence with light energy. Chin J Appl Environ Biol 22:1150–1155
Channatika K, Kanjana K, Saichol K, Doornet WGV (2015) Vesicles between plasma membrane and cell wall prior to visible senescence of Iris and Dendrobium flowers. J Plant Physiol 188:37–43
Wang H, Chang XX, Lin J, Chang YH, Chen JC, Reid MS, Jiang CZ (2018) Transcriptome profiling reveals regulatory mechanisms underlying corolla senescence in petunia. Hortic Res 5:16
Meeteren UV, Ieperen WV, Nijsse J, Keijzer K, Scheenen T, As HV (1999) Processes and xylem anatomical properties involved in rehydration dynamics of cut flowers. Acta Hortic 543:207–215
Solgi M, Kafi M, Taghavi TS, Naderi R (2009) Essential oils and silver nanoparticles (SNP) as novel agents to extend vase-life of gerbera (Gerbera jamesonii cv. 'Dune') flowers. Postharvest Biol Technol 53(3):155–158
Canchignia H, Altimira F, Montes C, Sánchez E, Tapia E, Miccono M et al (2017) Candidate nematicidal proteins in a new Pseudomonas veronii isolate identified by its antagonistic properties against Xiphinema index. J Gen Appl Microbiol 63(1):11–21
Hayward AC (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 29:65–87
Hulin MT, Mansfield JW, Brain P, Xu X, Jackson RW, Harrison RJ (2017) Characterization of the pathogenicity of strains of Pseudomonas syringae towards cherry and plum. Plant Pathol 67(5):1177–1193
Singh RK, Prasad M (2016) Advances in Agrobacterium tumefaciens-mediated genetic transformation of graminaceous crops. Protoplasma 253:691–707
Krenek P, Samajova O, Luptovciak I, Doskocilova A, Komi G, Samaj J (2015) Transient plant transformation mediated by Agrobacterium tumefaciens: principles, methods and applications. Biotechnol Adv 33(6):1024–1042
Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Cociancich S et al (2009) The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10:616
Xu ZY, Zou LF, Ma WX, Cai LL, Yang YY, Chen GY (2017) Action modes of transcription activator-like effectors (TALEs) of Xanthomonas in plants. J Integr Agric 16(12):2736–2745
Wulff NA, Mariano AG, Gaurivaud P, de Almeida Souza LC, Virgílio ACD, Monteiro PB (2008) Influence of culture medium pH on growth, aggregation, and biofilm formation of Xylella fastidiosa. Curr Microbiol 57(2):127–132
Casillo A, Ziaco M, Lindner B, Merino S, Mendoza-Barberá E, Tomás JM, Corsaro MM (2017) Structural characterization of core region in Erwinia amylovora lipopolysaccharide. Int J Mol Sci 18(3):559
Zhang Y, Kong J, Huang F, Xie YF, Guo YH, Cheng YL, Qian H, Yao WR (2018) Hexanal as a QS inhibitor of extracellular enzyme activity of Erwinia carotovora and Pseudomonas fluorescens and its application in vegetables. Food Chem 255:1–7
Afolabi O, Amoussa R, Bilé M, Oludare A, Gbogbo V, Poulin L, Koebnik R, Szurek B, Silué D (2016) First report of bacterial leaf blight of rice caused by Xanthomonas oryzae pv. oryzae in Benin. Plant Dis 100(2):515
Aksoy HM, Ozturk M, Aktas A (2017) First report of Pseudomonas viridiflava causing cabbage bacterial leaf spot in Turkey. J Plant Pathol 99:799–818
Khan ME, Khan MM, Min BK, Cho MH (2018) Microbial fuel cell assisted band gap narrowed TiO2 for visible light-induced photocatalytic activities and power generation. Sci Rep 8:1–12
Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964
Acknowledgments
We thank the anonymous reviewers and the editors for their constructive comments and suggestions to improve the manuscript. This work was supported by the National Key Research and Development Program of China (Grant No. 2017YFD0201301) and the Key Research and Development Program of Sichuan (Grant No. 2018NA0027).
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C.X.L. and Y.F.F. designed and performed most of the experiments, analyzed data, drafted, and revised the manuscript. W.L., Y.D., C.M.W., and M.X.W. participated in preparing and treating samples. Y.W., X.T., and P.M. analyzed and interpreted partial sequence data. X.R.M. conceived and designed research plan and experiments and supervised, critically revised, and complemented the writing. All authors read and approved the final manuscript.
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Li, CX., Fan, YF., Luan, W. et al. Titanium Ions Inhibit the Bacteria in Vase Solutions of Freshly Cut Gerbera jamesonii and Extend the Flower Longevity. Microb Ecol 77, 967–979 (2019). https://doi.org/10.1007/s00248-018-1273-2
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DOI: https://doi.org/10.1007/s00248-018-1273-2
Keywords
- Titanium ions
- Gerbera jamesonii
- Cut flower longevity
- Antibacterial activity
- High-throughput sequencing
- 16S rRNA gene
- V3-V4 variable regions