Abstract
Background and Aim
Increased soil salinization caused by natural or human activities is the leading cause of soil degradation. Cultivating salt-tolerant crops is an effective way to cope with soil salinity. However, the key salinity-tolerance traits and regulation mechanisms in salt-tolerant crops and the relevant ecological functions of the microbiome in the rhizosphere remain largely unexplored.
Methods
The phenotypic, physiological, morphological, and molecular responses of salt-sensitive (SS 212) and salt-tolerant (ST 47) broomcorn millet (Panicum miliaceum L.) to salinity were dissected, and the composition and variation in the rhizospheric microorganisms under saline and non-saline conditions were established.
Results
Salinity tolerance was achieved in ST 47 by maintaining Na+/K+ balance and intact cell surface and internal structures and regulating the expression of PmCNGC (Na+ uptake), PmNHX (Na+ sequestration), and PmSOS1 (Na+ extrusion). Moreover, the genotype mediated the differences in the rhizospheric microbial community. The ST 47 rhizosphere had a stronger and more stable fungal composition under saline conditions compared to SS 212. In addition, ST 47 reshaped the microorganisms in the rhizosphere by recruiting specific beneficial microbes, namely Haliangium, Marispirillum, RB41, and Saccharospirillum bacteria, which promote soil nutrient cycling, and Acremonium, Blastobotrys, Calostoma, Chaetomium, Chrysosporium, Fusarium, and Scytalidium fungi, which are involved in stress tolerance and resource uptake.
Conclusion
The findings of this study provide an empirical basis for improving crop performance through utilizing a key salt-tolerance mechanism and soil microbial management practices for sustainable agriculture in salinized soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that supports the findings of this study are available in the supplementary material of this article.
References
Ahmed V, Verma MK, Gupta S, Mandhan V, Chauhan NS (2018) Metagenomic profiling of soil microbes to mine salt stress tolerance genes. Front Microbiol 9:159. https://doi.org/10.3389/fmicb.2018.00159
Albaladejo I, Meco V, Plasencia F, Flores FB, Bolarin MC, Egea I (2017) Unravelling the strategies used by the wild tomato species Solanum pennellii to confront salt stress: From leaf anatomical adaptations to molecular responses. Environ Exp Bot 135:1–12. https://doi.org/10.1016/j.envexpbot.2016.12.003
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Bhanbhro N, Xiao BB, Han L, Lu HY, Wang H, Yang CW (2020) Adaptive strategy of allohexaploid wheat to long-term salinity stress. BMC Plant Biol 20:1. https://doi.org/10.1186/s12870-020-02423-2
Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep-Uk 6:34768. https://doi.org/10.1038/srep34768
Brancalion PHS, Guillemot J, Cesar RG, Andrade HS, Mendes A, Sorrini TB, Piccolo MDC, Peluci MC, Moreno VDS, Colletta G, Chazdon RL (2020) The cost of restoring carbon stocks in Brazil’s Atlantic Forest. Land Degrad Dev 32:830–841. https://doi.org/10.1002/ldr.3764
Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33. https://doi.org/10.1017/S0021859600021572
Caporaso JG, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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, Tumbaugh 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. https://doi.org/10.1038/nmeth.f.303
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. https://doi.org/10.1111/nph.13697
Cuevas J, Daliakopoulos IN, del Moral F, Hueso JJ, Tsanis IK (2019) A review of soil-improving cropping systems for soil salinization. Agronomy-Basel 9:295. https://doi.org/10.3390/agronomy9060295
de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P, Lumini E, Mason KE, Oliver A, Ostle N, Prosser JI, Thion C, Thomson B, Bardgett RD (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033. https://doi.org/10.1038/s41467-018-05516-7
Deinlein U, Stephan AB, Horie T, Luo W, Xu GH, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Dong ZY, Rao MPN, Wang HF, Fang BZ, Liu YH, Li L, Xiao M, Li WJ (2019) Transcriptomic analysis of two endophytes involved in enhancing salt stress ability of Arabidopsis thaliana. Sci Total Environ 686:107–117. https://doi.org/10.1016/j.scitotenv.2019.05.483
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/NMETH.2604
Egidi E, Delgado-Baquerizo M, Plett JM, Wang JT, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK (2019) A few Ascomycota taxa dominate soil fungal communities worldwide. Nat Commun 10:2369. https://doi.org/10.1038/s41467-019-10373-z
Eswar D, Karuppusamy R, Chellamuthu S (2021) Drivers of soil salinity and their correlation with climate change. Curr Opin Env Sust 50:310–318. https://doi.org/10.1016/j.cosust.2020.10.015
Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2:6. https://doi.org/10.1186/2049-2618-2-6
Fehrer J, Reblova M, Bambasova V, Vohnik M (2019) The root-symbiotic Rhizoscyphus ericae aggregate and Hyaloscypha (Leotiomycetes) are congeneric: Phylogenetic and experimental evidence. Stud Mycol 92:195–225. https://doi.org/10.1016/j.simyco.2018.10.004
Finkel OM, Castrillo G, Paredes SH, Gonzalez IS, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163. https://doi.org/10.1016/j.pbi.2017.04.018
Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot-London 115:419–431. https://doi.org/10.1093/aob/mcu217
Habiyaremye C, Matanguihan JB, Guedes JD, Ganjyal GM, Whiteman MR, Kidwell KK, Murphy KM (2017) Proso millet (Panicum miliaceum L.) and its potential for cultivation in the pacific northwest, U. S.: A review. Front Plant Sci 7:1961. https://doi.org/10.3389/fpls.2016.01961
Hayat K, Zhou YF, Menhas S, Bundschuh J, Hayat S, Ullah A, Wang JC, Chen XF, Zhang D, Zhou P (2020) Pennisetum giganteum: An emerging salt accumulating/tolerant non-conventional crop for sustainable saline agriculture and simultaneous phytoremediation. Environ Pollut 265:114876. https://doi.org/10.1016/j.envpol.2020.114876
Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: A systems biology perspective. Front Plant Sci 8:1768. https://doi.org/10.3389/fpls.2017.01768
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. https://doi.org/10.1007/s11104-011-0877-9
Jiang JY, Li ZW, Xiao HB, Wang DY, Liu C, Zhang XQ, Peng H, Zeng GM (2019) Labile organic matter plays a more important role than the autotrophic bacterial community in regulating microbial CO2 fixation in an eroded watershed. Land Degrad Dev 29:4415–4423. https://doi.org/10.1002/ldr.3182
Kanehiro Y, Sherman GD (1965) Fusion with sodium carbonate for total elemental analysis. In: Black CA (ed) Methods of soil analysis, Part 2, agronomy 9. American Society of Agronomy, Inc., Madison, pp 952–958
Kearl J, McNary C, Lowman JS, Mei CS, Aanderud ZT, Smith ST, West J, Colton E, Hamson M, Nielsen BL (2019) Salt-tolerant halophyte rhizosphere bacteria stimulate growth of alfalfa in salty soil. Front Microbiol 10:1849. https://doi.org/10.3389/fmicb.2019.01849
Li D, Ni HW, Jiao S, Lu YH, Zhou JZ, Sun B, Liang YT (2021a) Coexistence patterns of soil methanogens are closely tied to methane generation and community assembly in rice paddies. Microbiome 9:20. https://doi.org/10.1186/s40168-020-00978-8
Li H, La SK, Zhang X, Gao LH, Tian YQ (2021b) Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress. ISME J 15:2865–2882. https://doi.org/10.1038/s41396-021-00974-2
Lian TX, Huang YY, Xie XN, Huo X, Shahid MQ, Tian L, Lan T, Jin J (2020) Rice SST variation shapes the rhizosphere bacterial community, conferring tolerance to salt stress through regulating soil metabolites. Msystems 5:e00721-20. https://doi.org/10.1128/mSystems.00721-20
Litalien A, Zeeb B (2020) Curing the earth: A review of anthropogenic soil salinization and plant-based strategies for sustainable mitigation. Sci Total Environ 698:134235. https://doi.org/10.1016/j.scitotenv.2019.134235
Liu MX, Qiao ZJ, Zhang S, Wang YY, Lu P (2015) Response of broomcorn millet (Panicum miliaceum L.) genotypes from semiarid regions of China to salt stress. Crop J 3:57–66. https://doi.org/10.1016/j.cj.2014.08.006
Liu TZ, Zhuang LL, Huang BR (2019) Metabolic adjustment and gene expression for root sodium transport and calcium signaling contribute to salt tolerance in Agrostis grass species. Plant Soil 443:219–232. https://doi.org/10.1007/s11104-019-04140-8
Liu MM, Pan T, Allakhyerdiev SI, Yu M, Shabala S (2020) Crop halophytism: An environmentally sustainable solution for global food security. Trends Plant Sci 25:630–634. https://doi.org/10.1016/j.tplants.2020.04.008
Liu BB, Wang XX, Li K, Cai ZW (2021) Spatially resolved metabolomics and lipidomics reveal salinity and drought-tolerant mechanisms of cottonseeds. J Agr Food Chem 69:8028–8037. https://doi.org/10.1021/acs.jafc.1c01598
Lowry DB, Hall MC, Salt DE, Willis JH (2009) Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol 183:776–788. https://doi.org/10.1111/j.1469-8137.2009.02901.x
Lozupone C, Hamady M, Knight R (2006) UniFrac-An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371. https://doi.org/10.1186/1471-2105-7-371
Lu J, Wu J, Zhang C (2021) Cleaner production of salt-tolerance vegetable in coastal saline soils using reclaimed water irrigation: Observations from alleviated accumulation of endocrine disrupting chemicals and environmental burden. J Clean Prod 297:126746. https://doi.org/10.1016/j.jclepro.2021.126746
Luan CG, Xie LL, Yang X, Miao HF, Lv N, Zhang RF, Xiao X, Hu YF, Liu YL, Zhu BL (2015) Dysbiosis of fungal microbiota in the intestinal mucosa of patients with colorectal adenomas. Sci Rep-Uk 5:7980. https://doi.org/10.1038/srep07980
Ma LY, Zhang H, Sun LR, Jiao YH, Zhang GZ, Miao C, Hao FS (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317. https://doi.org/10.1093/jxb/err280
Maddhesiya PK, Singh K, Singh RP (2021) Effects of perennial aromatic grass species richness and microbial consortium on soil properties of marginal lands and on biomass production. Land Degrad Dev 32:1008–1021. https://doi.org/10.1002/ldr.3742
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Mhlongo MI, Piater LA, Madala NE, Labuschagne N, Dubery IA (2018) The chemistry of plant-microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front Plant Sci 9:112. https://doi.org/10.3389/fpls.2018.00112
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
Munns R, Gilliham M (2015) Salinity tolerance of crops - what is the cost? New Phytol 208:668–673. https://doi.org/10.1111/nph.13519
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Muthamilarasan M, Prasad M (2021) Small millets for enduring food security amidst pandemics. Trends Plant Sci 26:33–40. https://doi.org/10.1016/j.tplants.2020.08.008
Naumoff DG, Dedysh SN (2012) Lateral gene transfer between the Bacteroidetes and Acidobacteria: The case of alpha-L-rhamnosidases. FEBS Lett 586:3843–3851. https://doi.org/10.1016/j.febslet.2012.09.005
Ngamnikom P, Songsermpong S (2011) The effects of freeze, dry, and wet grinding processes on rice flour properties and their energy consumption. J Food Eng 104:632–638. https://doi.org/10.1016/j.jfoodeng.2011.02.001
Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Carrasco KBR, Martinez EA, Alnayef M, Marotti I, Bosi S (2011) Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol 38:818–831. https://doi.org/10.1071/FP11088
Qin Y, Druzhinina IS, Pan XY, Yuan ZL (2016) Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol Adv 34:1245–1259. https://doi.org/10.1016/j.biotechadv.2016.08.005
Rajput SG, Santra DK (2016) Evaluation of genetic diversity of proso millet germplasm available in the United States using simple-sequence repeat markers. Crop Sci 56:2401–2409. https://doi.org/10.2135/cropsci2015.10.0644
Rodriguez PA, Rothballer M, Chowdhury SP, Nussbaumer T, Gutjahr C, Falter-Braun P (2019) Systems biology of plant-microbiome interactions. Mol Plant 12:804–821. https://doi.org/10.1016/j.molp.2019.05.006
Saleh ASM, Zhang Q, Chen J, Shen Q (2013) Millet Grains: Nutritional quality, processing, and potential health benefits. Compr Rev Food Sci F 12:281–295. https://doi.org/10.1111/1541-4337.12012
Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot-London 112:1209–1221. https://doi.org/10.1093/aob/mct205
Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhou DW, Shabala S (2012) Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiol Plantarum 146:26–38. https://doi.org/10.1111/j.1399-3054.2012.01599.x
Shehzad M, Zhou ZL, Ditta A, Cai XY, Khan M, Xu YC, Hou YQ, Peng RH, Hao FS, Shafeeq-ur-rahman Wang KB, Liu F (2019) Genome-wide mining and identification of protein kinase gene family impacts salinity stress tolerance in highly dense genetic map developed from interspecific cross between G. hirsutum L. and G. darwinii G. Watt. Agronomy-Basel 9:9. https://doi.org/10.3390/agronomy9090560
Shi JP, Ma XX, Zhang JH, Zhou YS, Liu MX, Huang LL, Su SL, Zhang XB, Gao X, Zhan W, Li PH, Wang L, Lu P, Zhao HM, Song WB, Lai JS (2019) Chromosome conformation capture resolved near complete genome assembly of broomcorn millet. Nat Commun 10:464–477. https://doi.org/10.1038/s41467-018-07876-6
Singh K (2016) Microbial and enzyme activities of saline and sodic soils. Land Degrad Dev 27:706–718. https://doi.org/10.1002/ldr.2385
Soldan R, Mapelli F, Crotti E, Schnell S, Daffonchio D, Marasco R, Fusi M, Borin S, Cardinale M (2019) Bacterial endophytes of mangrove propagules elicit early establishment of the natural host and promote growth of cereal crops under salt stress. Microbiol Res 223:33–43. https://doi.org/10.1016/j.micres.2019.03.008
Sun Y, Chen HYH, Jin L, Wang CT, Zhang RT, Ruan HH, Yang JY (2020) Drought stress induced increase of fungi: bacteria ratio in a poplar plantation. Catena 193:104607. https://doi.org/10.1016/j.catena.2020.104607
Trivedi P, Leach JE, Tringe SG, Sa TM, Singh BK (2020) Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621. https://doi.org/10.1038/s41579-020-0412-1
Troost TA, Kooi BW, Kooijman SALM (2005) When do mixotrophs specialize? Adaptive dynamics theory applied to a dynamic energy budget model. Math Biosci 193:159–182. https://doi.org/10.1016/j.mbs.2004.06.010
van Zelm E, Zhang YX, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718-100005
Venceslau SS, Lino RR, Pereira IAC (2010) The Qrc membrane complex, related to the alternative complex iii, is a menaquinone reductase involved in sulfate respiration. J Biol Chem 285:22772–22781. https://doi.org/10.1074/jbc.M110.124305
Ventura F, Vignudelli M, Poggi GM, Negri L, Dinelli G (2020) Phenological stages of proso millet (Panicum miliaceum L.) encoded in BBCH scale. Int J Biometeorol 64:1167–1181. https://doi.org/10.1007/s00484-020-01891-3
Walker TW, Adams AFR (1958) Influence of phosphorous content of parent materials on accumulation of carbon, nitrogen, sulphur, and organic phosphorous in grassland soils. Soil Sci 85:307–318. https://doi.org/10.1097/00010694-195806000-00004
Walkley AJ, Black IA (1934) An examination of the degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38
Wang R, Zhang HC, Sun LG, Qi GF, Chen S, Zhao XY (2017) Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Sci Rep-Uk 7:343. https://doi.org/10.1038/s41598-017-00472-6
Wang NN, Li L, Zhang BW, Chen SP, Sun W, Luo YK, Dong KH, Han XG, Huang JH, Xu XF, Wang CH (2020) Population turnover promotes fungal stability in a semi-arid grassland under precipitation shifts. J Plant Ecol 13:499–509. https://doi.org/10.1093/jpe/rtaa038
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz NM, Venables B, Galili T (2013) gplots: Various R programming tools for plotting data. R package version 2.12.1. Available at: http://cran.r-project.org/web/packages/gplots/index.html. Accessed 30 Sept 2014
Yao Z, Yaeger R, Rodrik-Outmezguine VS, Tao A, Torres NM, Chang MT, Drosten M, Zhao HY, Cecchi F, Hembrough T, Michels J, Baumert H, Miles L, Campbell NM, de Stanchina E, Solit DB, Barbacid M, Taylor BS, Rosen N (2017) Tumours with class 3 BRAF mutants are sensitive to the inhibition of activated RAS. Nature 548:234–238. https://doi.org/10.1038/nature23291
Yuan YH, Li J, Ma HC, Yang QH, Liu CJ, Feng BL (2020) Salt-tolerant broomcorn millet (Panicum miliaceum L.) resists salt stress via modulation of cell wall biosynthesis and Na+ balance. Land Degrad Dev 32:518–532. https://doi.org/10.1002/ldr.3717
Yuan YH, Liu JJ, Ma Q, Gao YB, Yang QH, Gao XL, Feng BL (2022) Cleaner production of proso millet (Panicum miliaceum L.) in salt-stressed environment using re-watering: From leaf structural alleviations to multi-omics responses. J Clean Prod 334:130205. https://doi.org/10.1016/j.jclepro.2021.130205
Yue YS, Zhang MC, Zhang JC, Duan LS, Li ZH (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. J Plant Physiol 169:255–261. https://doi.org/10.1016/j.jplph.2011.10.007
Yue H, Deng PC, Liu SY, Wang M, Song WN, Nie XJ (2016) Selection and evaluation of reference genes for quantitative gene expression analysis in broomcorn millet (Panicum miliaceum L.). J Plant Biol 59:435–443. https://doi.org/10.1007/s12374-016-0024-5
Zhang J, Yu HY, Zhang YS, Wang YB, Li MY, Zhang JC, Duan LS, Zhang MC, Li ZH (2016) Increased abscisic acid levels in transgenic maize overexpressing AtLOS5 mediated root ion fluxes and leaf water status under salt stress. J Exp Bot 67:1339–1355. https://doi.org/10.1093/jxb/erv528
Zhang H, Zhao Y, Zhu JK (2020) Thriving under stress: how plants balance growth and the stress response. Dev Cell 55(5):529–543. https://doi.org/10.1016/j.devcel.2020.10.012
Zhao CZ, Zhang H, Song CP, Zhu JK, Shabala S (2020a) Mechanisms of plant responses and adaptation to soil salinity. Innovation 1:100017. https://doi.org/10.1016/j.xinn.2020.100017
Zhao S, Liu JJ, Banerjee S, Zhou N, Zhao ZY, Zhang K, Hu MF, Tian CY (2020b) Biogeographical distribution of bacterial communities in saline agricultural soil. Geoderma 361:114095. https://doi.org/10.1016/j.geoderma.2019.114095
Zhao FZ, Maren NA, Kosentka PZ, Liao YY, Lu HY, Duduit JR, Huang DB, Ashrafi H, Zhao TJ, Huerta AI, Ranney TG, Liu W (2021) An optimized protocol for stepwise optimization of real-time RT-PCR analysis. Hortic Res-England 8:179. https://doi.org/10.1038/s41438-021-00616-w
Zheng YF, Xu ZC, Liu HD, Liu Y, Zhou YN, Meng C, Ma SQ, Xie ZH, Li YQ, Zhang CS (2021) Patterns in the microbial community of salt-tolerant plants and the functional genes associated with salt stress alleviation. Microbiol Spectr 9:e00767. https://doi.org/10.1128/Spectrum.00767-21
Zhu JY, Zhu H, Cao YJ, Li JH, Zhu QY, Yao JM, Xu CY (2020) Effect of simulated warming on leaf functional traits of urban greening plants. BMC Plant Biol 20:139. https://doi.org/10.1186/s12870-020-02359-7
Zörb C, Geilfus CM, Dietz KJ (2019) Salinity and crop yield. Plant Biol 21:31–38. https://doi.org/10.1111/plb.12884
Zou CS, Li LT, Miki D, Li DL, Tang QM, Xiao LH, Rajput S, Deng P, Peng L, Jia W, Huang R, Zhang ML, Sun YD, Hu JM, Fu X, Schnable PS, Chang YX, Li F, Zhang H, Feng BL, Zhu XG, Liu RY, Schnable JC, Chnable JC, Zhu JK, Zhang H (2019) The genome of broomcorn millet. Nat Commun 10:436. https://doi.org/10.1038/s41467-019-08409-5
Acknowledgements
This work was financially supported by the Minor Grain Crops Research and Development System of Shaanxi Province (NYKJ-2021-YL [XN] 40) and the China Agriculture Research System (CARS-06-A26).
Author information
Authors and Affiliations
Contributions
Yuhao Yuan: Methodology, Formal analysis, Visualization, Writing-original draft. Jiang Li: Investigation, Data curation, Writing-review & editing. Miaomiao Zhang: Conceptualization, Resources. Qinghua Yang: Validation, Writing-review & editing. Baili Feng: Supervision, Funding acquisition.
Corresponding authors
Ethics declarations
Competing interest
The authors declare that they have no competing financial interests or personal relationships that could affect the work described in this article.
Additional information
Responsible Editor: Janusz J. Zwiazek.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yuan, Y., Li, J., Zhang, M. et al. Broomcorn millet (Panicum miliaceum L.) tolerates soil salinity by regulating salt-tolerance mechanism and reshaping rhizosphere microorganisms. Plant Soil 492, 261–284 (2023). https://doi.org/10.1007/s11104-023-06170-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06170-9