Assessment of Rhizosphere Microbial Community Structure in Tomato Plants after Inoculation of Bacillus Species for Inducing Tolerance to Salinity |
Yoo, Sung-Je
(Division of Agricultural Microbiology, Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration)
Lee, Shin Ae (Division of Agricultural Microbiology, Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) Weon, Hang-Yeon (Division of Agricultural Microbiology, Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) Song, Jaekyeong (Division of Agricultural Microbiology, Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) Sang, Mee Kyung (Division of Agricultural Microbiology, Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) |
1 | Yoo SJ, Shin DJ, Weon HY, Song J, Sang MK (2018) Selection of bacteria for enhancement of tolerance to salinity and temperature stresses in tomato plants. Korean Journal of Organic Agriculture, 26, 463-475. DOI |
2 | Polonenko DR, Mayfield CI, Dumbroff EB (1981) Microbial responses to salt-induced osmotic stress. Plant and Soil, 59, 269-285. DOI |
3 | Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clement C, Fontaine F, Ait Barka E (2012) Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Molecular Plant-Microbe Interactions, 25, 496-504. https://doi.org/10.1094/MPMI-09-11-0245. DOI |
4 | Lichtenthaler HK (1987) Chlorophyll fluorescence signatures of leaves during the autumnal chlorophyll breakdown. Journal of Plant Physiology, 131, 101-110. https://doi.org/10.1016/S0176-1617(87)80271-7. DOI |
5 | Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205-207. https://doi.org/10.1007/BF00018060. DOI |
6 | Tiwari S, Prasad V, Chauhan PS, Lata C (2017) Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Frontiers in Plant Science, 8, 1510. https://doi.org/10.3389/fpls.2017.01510. DOI |
7 | Liu RX, Zhou ZG, Guo WQ, Chen BL, Oosterhuis DM (2008) Effects of N fertilization on root development and activity of water-stressed cotton (Gossypium hirsutum L.) plants. Agricultural Water Management, 95, 1261-1270. DOI |
8 | Cho HS, Seo MC, Kim JH, Sang WG, Shin P, Baek JK (2018) The changes of soil carbon as affected by several kinds of organic material in upland soil. Korean Journal of Soil Science and Fertilizer, 51, 586-595. DOI |
9 | Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537-7541. DOI |
10 | Qiao Q, Wang F, Zhang J, Chen Y, Zhang C, Liu G, Zhang J (2017) The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Scientific Reports, 7, 3940. https://doi.org/10.1038/s41598-017-04213-7. DOI |
11 | Ruiz-Sola MA, Arbona V, Gomez-Cadenas A, Rodriguez-Concepcion M, Rodriguez-Villalon A (2014) A root specific induction of carotenoid biosynthesis contributes to ABA production upon salt stress in Arabidopsis. PLoS ONE, 9, e90765. https://doi.org/10.1371/journal. pone.0090765. DOI |
12 | Badri DV, Chaparro JM, Zhang RF, Shen QR, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry, 288, 4502-4512. https://doi.org/10.1074/jbc.M112.433300. DOI |
13 | Kong XQ, Wang T, Li WJ, Tang W, Zhang DM, Dong, HZ (2016) Exogenous nitric oxide delays salt-induced leaf senescence in cotton (Gossypium hirsutum L.). Acta Physiologiae Plantarum, 38, 61. DOI |
14 | Turan S, Tripathy BC (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiologia Plantarum, 153, 477-491. https://doi.org/10.1111/ppl.12250. DOI |
15 | Jamil M, Lee KJ, Kim JM, Kim HS, Rha, ES (2007) Salinity reduced growth PS2 photochemistry and chlorophyll content in radish. Scientia Agricola, 64, 111-118. https://doi.org/10.1590/S0103-90162007000200002. DOI |
16 | Soti PG, Jayachandran K, Koptur S, Volin JC (2015) Effect of soil pH on growth, nutrient uptake, and mycorrhizal colonization in exotic invasive Lygodium microphyllum. Plant Ecology, 216, 989-998. https://doi.org/10.1007/s11258-015-0484-6. DOI |
17 | Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: A review. Plant Signaling and Behavior, 7, 1456-1466. https://doi.org/10.4161/psb.21949. DOI |
18 | Ben Rejeb K, Abdelly C, Savoure A (2014) How reactive oxygen species and proline face stress together. Plant Physiology and Biochemistry, 80, 278-284. https:// doi.org/10.1016/j.plaphy.2014.04.007. DOI |
19 | Sevengor S, Yasar F, Kusvuran S, Ellialtioglu S (2011) The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling. African Journal of Agricultural Research, 6, 4920-4924. |
20 | Tsikas D (2017) Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: Analytical and biological challenges. Analytical Biochemistry, 524, 13-30. https://doi.org/10.1016/j.ab.2016.10.021. DOI |
21 | De Boer W, Kowalchuk G (2001) Nitrification in acid soils: Micro-organisms and mechanisms. Soil Biology and Biochemistry, 33, 853-866. https://doi.org/10.1016/S0038-0717(00)00247-9. DOI |
22 | Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology, 10, 2966-2978. https://doi.org/10.1111/j.1462-2920.2008.01701.x. DOI |
23 | Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiology and Biochemistry, 66, 1-9. https://doi.org/10.1016/j.plaphy.2013.01.020. DOI |
24 | Shamshiri RR, Jones JW, Thorp KR, Ahmad D, Man HC, Taheri S (2018) Review of optimum temperature, humidity, and vapour pressure deficit for microclimate evaluation and control in greenhouse cultivation of tomato: A review. International Agrophysics, 32, 287-302. https://doi.org/10.1515/intag-2017-0005. DOI |
25 | Dawson W, Hor J, Egert M, Kleunen VM, Pester M (2017) A small number of low-abundance bacteria dominate plant species-specific responses during rhizosphere colonization. Frontiers in Microbiology, 8, 975. https://doi.org/10.3389/fmicb.2017.00975. DOI |
26 | Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, Kusel K, Rillig MC, Rivett DW (2017) Where less may be more: how the rare biosphere pulls ecosystems strings. The ISME Journal, 11, 853-862. https://doi.org/10.1038/ismej.2016.174. DOI |
27 | Yurkov A, Guerreiro MA, Sharma L, Carvalho C, Fonseca A (2015) Multigene assessment of the species boundaries and sexual status of the basidiomycetous yeasts Cryptococcus flavescens and C. Terrestris (tremellales). PLoS One, 10, e0120400. https://doi.org/10.1371/journal.pone.0120400. DOI |
28 | Willcox JK, Catignani GL, Lazarus S (2003) Tomatoes and cardiovascular health. Critical Reviews in Food Science and Nutrition, 43, 1-18. https://doi.org/10.1080/10408690390826437. DOI |
29 | Gerszberg A, Hnatuszko-Konka K, Kowalczyk T, Kononowicz AK (2015) Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell, Tissue and Organ Culture (PCTOC), 120, 881-902. https://doi.org/10.1007/s11240-014-0664-4. DOI |
30 | Ayyogari K, Sidhya P, Pandit MK (2014) Impact of climate change on vegetable cultivation - a review. International Journal of Agriculture, Environment and Biotechnology, 7(1), 145-155. https://doi.org/10.5958/j.2230-732X.7.1.020. DOI |
31 | Zongsuo L, Zhongrong D, Shaotang W (1992) Study on types of water stress adaptation in both Brassica napus L. and Brassica juncea L. Acta Botanica Borealioccidentalia Sinica, 01. |
32 | Shrivastava P, Kumar R (2015) Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences, 22(2), 123-131. https://doi.org/10.1016/j.sjbs.2014.12.001. DOI |
33 | Bharti N, Barnawal D, Maji D, Kalra, A (2015) Halotolerant PGPRs prevent major shifts in indigenous microbial community structure under salinity stress. Microbial Ecology, 70(1), 196-208. https://doi.org/10.1007/s00248-014-0557-4. DOI |
34 | Moreno-Limon S, Maiti RK, Nunez-Gonzalez A, Star JV, Foroughbakhch R, Gamez-Gonzalez H (2000) Genotypic variability in bean cultivars (Phaseolus vulgaris L.) for resistance to salinity at the seedling stage. Indian Agriculturist, 44, 1-12. |
35 | El-Esawi MA, Alaraidh IA, Alsahli AA, Alzahrani SM, Ali HM, Alayafi A, Ahmad M (2018) Serratia liquefaciens KM4 improves salt stress tolerance in maize by regulating redox potential, ion homeostasis, leaf gas exchange and stress-related gene expression. International Journal of Molecular Science, 19, 3310. https://doi.org/10.3390/ijms19113310. DOI |
36 | Li HW, Zang BS, Deng XW, Wang XP (2011) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta, 234(5), 1007-1018. https://doi.org/10.1007/s00425-011-1458-0. DOI |
37 | Munoz-Mayor A, Pineda B, Garcia-Abellan JO, Anton T, GarciaSogo B, Sanchez-Bel P, Flores FB, Atares A, Angosto T, PintorToro JA, Moreno V, Bolarin MC (2012) Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. Journal of Plant Physiology, 169, 459-468. https://doi.org/10.1016/j.jplph.2011.11.018. DOI |
38 | Putranta H, Permatasari AK, Sukma TA, Suparno, Dwandaru WSB (2019) The effect of pH, electrical conductivity, and nitrogen (N) in the soil at Yogyakarta special region on tomato plant growth. TEM Journal, 8(3), 860-865. |
39 | Chen L, Liu Y, Wu G, Veronican Njeri K, Shen Q, Zhang N, Zhang R (2016) Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiologia Plantarum, 158(1), 34-44. https://doi.org/10.1111/ppl.12441. DOI |
40 | Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World Journal of Microbiology and Biotechnology, 28(4), 1327-1350. https://doi.org/10.1007/s11274-011-0979-9. DOI |
41 | Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, Shen Q (2017) Inducing the rhizosphere microbiome by biofertilizer application to suppress banana fusarium wilt disease. Soil Biology and Biochemistry, 104, 39-48. https://doi.org/10.1016/j.soilbio.2016.10.008. DOI |
42 | Silini A, Cherif-Silini H, Yahiaoui B (2016) Growing varieties durum wheat (Triticum durum) in response to the effect of osmolytes and inoculation by Azotobacter chroococcum under salt stress. African Journal of Microbiology Research, 10(12), 387-399. https://doi.org/10.5897/AJMR2015.7723. DOI |
43 | Akram MS, Shahid M, Tariq M, Azeem M, Javed MT, Saleem S, Riaz S (2016) Deciphering Staphylococcus sciuri SAT-17 mediated anti-oxidative defense mechanisms and growth modulations in salt stressed maize (Zea mays L.). Frontiers in Microbiology, 7, 867. https://doi.org/10.3389/fmicb.2016.00867. DOI |
44 | Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 37(5), 634-663. https://doi.org/10.1111/1574-6976.12028. DOI |
45 | Chihaoui SA, Trabelsi D, Jdey A, Mhadhbi H, Mhamdi R. (2015) Inoculation of Phaseolus vulgaris with the nodule-endophyte Agrobacterium sp. 10C2 affects richness and structure of rhizosphere bacterial communities and enhances nodulation and growth. Archives of Microbiology, 197, 805-813. https://doi.org/10.1007/s00203-015-1118-z. DOI |
46 | Xue L, Ren H, Li S, Leng X, Yao X (2017) Soil bacterial community structure and co-occurrence pattern during vegetation restoration in karst rocky desertification area. Frontiers in Microbiology, 8, 2377. https://doi.org/10.3389/fmicb.2017.02377. DOI |
47 | Bharti N, Barnawal D, Wasnik K, Tewari SK, Kalra A (2016) Co-inoculation of Dietzia natronolimnaea and Glomus intraradices with vermicompost positively influences Ocimum basilicum growth and resident microbial community structure in salt affected low fertility soils. Applied Soil Ecology, 100, 211-225. https://doi.org/10.1016/j.apsoil.2016.01.003. DOI |
48 | Yoo SJ, Weon HY, Song J, Sang MK (2019) Induced tolerance to salinity stress by halotolerant bacteria Bacillus aryabhattai H19-1 and B. Mesonae H20-5 in tomato plants. Journal of Microbiology and Biotechnology, 29(7), 1124-1136. https://doi.org/10.4014/jmb.1904.04026. DOI |
49 | Vacheron J, Moenne-Loccoz Y, Dubost A, Goncalves-Martins M, Muller D, Prigent-Combaret C (2016) Fluorescent Pseudomonas strains with only few plant-beneficial properties are favored in the maize rhizosphere. Frontiers in Plant Science, 7, 1212. https://doi.org/10.3389/fpls.2016.01212. DOI |
50 | Piromyou P, Buranabanyat B, Tantasawat P, Tittabutr P, Boonkerd N, Teaumroong N (2011) Effect of plant growth promoting rhizobacteria (PGPR) inoculation on microbial community structure in rhizosphere of forage corn cultivated in Thailand. European Journal of Soil Biology, 47(1), 44-54. https://doi.org/10.1016/j.ejsobi.2010.11.004. DOI |