Abstract
Key message
We studied the salt stress tolerance of two accessions isolated from different areas of the world (Norway and Tunisia) and characterized the mechanism(s) regulating salt stress in Brachypodium sylvaticum Osl1 and Ain1.
Abstract
Perennial grasses are widely grown in different parts of the world as an important feedstock for renewable energy. Their perennial nature that reduces management practices and use of energy and agrochemicals give these biomass crops advantages when dealing with modern agriculture challenges such as soil erosion, increase in salinized marginal lands and the runoff of nutrients. Brachypodium sylvaticum is a perennial grass that was recently suggested as a suitable model for the study of biomass plant production and renewable energy. However, its plasticity to abiotic stress is not yet clear. We studied the salt stress tolerance of two accessions isolated from different areas of the world and characterized the mechanism(s) regulating salt stress in B. sylvaticum Osl1, originated from Oslo, Norway and Ain1, originated from Ain-Durham, Tunisia. Osl1 limited sodium transport from root to shoot, maintaining a better K/Na homeostasis and preventing toxicity damage in the shoot. This was accompanied by higher expression of HKT8 and SOS1 transporters in Osl1 as compared to Ain1. In addition, Osl1 salt tolerance was accompanied by higher abundance of the vacuolar proton pump pyrophosphatase and Na+/H+ antiporters (NHXs) leading to a better vacuolar pH homeostasis, efficient compartmentation of Na+ in the root vacuoles and salt tolerance. Although preliminary, our results further support previous results highlighting the role of Na+ transport systems in plant salt tolerance. The identification of salt tolerant and sensitive B. sylvaticum accessions can provide an experimental system for the study of the mechanisms and regulatory networks associated with stress tolerance in perennials grass.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aghaleh M, Niknam V, Ebrahimzadeh H, Razavi K (2009) Salt stress effects on growth, pigments, proteins and lipid peroxidation in Salicornia persica and S. europaea. Biol Plant 53:243–248. https://doi.org/10.1007/s10535-009-0046-7
Apse MP, Blumwald E (2007) Na+ transport in plants. Febs Lett 581(12):2247–2254. https://doi.org/10.1016/j.febslet.2007.04.014
Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285(5431):1256–1258. https://doi.org/10.1126/science.285.5431.1256
Ayala-Astorga G, Alcaraz-Meléndez L (2010) Salinity effects on protein content, lipid peroxidation, pigments, and proline in Paulownia imperialis (Siebold & Zuccarini) and Paulownia fortunei (Seemann & Hemsley) grown in vitro. Electron J Biotechnol. https://doi.org/10.2225/vol13-issue5-fulltext-13
Bao AK, Du BQ, Touil L, Kang P, Wang QL, Wang SM (2016) Co-expression of tonoplast cation/H+ antiporter and H+-pyrophosphatase from xerophyte Zygophyllum xanthoxylum improves alfalfa plant growth under salinity, drought and field conditions. Plant Biotechnol J 14(3):964–975. https://doi.org/10.1111/pbi.12451
Bassil E, Tajima H, Liang YC, Ohto M, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011a) The Arabidopsis Na(+)/H(+) antiporters NHX1 and NHX2 control vacuolar pH and K(+) homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23(9):3482–3497. https://doi.org/10.1105/tpc.111.089581
Bassil E, Tajima H, Liang YC, Ohto M, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011b) The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23(9):3482–3497. https://doi.org/10.1105/tpc.111.089581
Bassil E, Krebs M, Halperin S, Schumacher K, Blumwald E (2013) Fluorescent dye based measurement of vacuolar pH and K+. Bio-Protocol. https://doi.org/10.21769/BioProtoc.810. http://www.bio-protocol.org/e810
Bhaskaran S, Savithramma DL (2011) Co-expression of Pennisetum glaucum vacuolar Na+/H+ antiporter and Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic tomato. J Exp Bot 62(15):5561–5570. https://doi.org/10.1093/jxb/err237
Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12(4):431–434. https://doi.org/10.1016/s0955-0674(00)00112-5
Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1006/abio.1976.9999
Brkljacic J, Grotewold E, Scholl R, Mockler T, Garvin DF, Vain P, Brutnell T, Sibout R, Bevan M, Budak H, Caicedo AL, Gao CX, Gu Y, Hazen SP, Holt BF, Hong SY, Jordan M, Manzaneda AJ, Mitchell-Olds T, Mochida K, Mur LAJ, Park CM, Sedbrook J, Watt M, Zheng SJ, Vogel JP (2011) Brachypodium as a model for the grasses: today and the future. Plant Physiol 157(1):3–13. https://doi.org/10.1104/pp.111.179531
Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143(4):1918–1928. https://doi.org/10.1104/pp.093476
Caldana C, Degenkolbe T, Cuadros-Inostroza A, Klie S, Sulpice R, Leisse A, Steinhauser D, Fernie AR, Willmitzer L, Hannah MA (2011) High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant J 67(5):869–884. https://doi.org/10.1111/j.1365-313X.2011.04640.x
Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–182. https://doi.org/10.1146/annurev.arplant.043008.092125
Chevallet M, Luche S, Rabilloud T (2006) Silver staining of proteins in polyacrylamide gels. Nat Protoc 1(4):1852–1858. https://doi.org/10.1038/nprot.2006.288
Cuadros-Inostroza A, Caldana C, Redestig H, Kusano M, Lisec J, Pena-Cortes H, Willmitzer L, Hannah MA (2009) TargetSearch: a bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinform. https://doi.org/10.1186/1471-2105-10-428
Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30(4):497–507. https://doi.org/10.1111/j.1365-3040.2007.01637.x
Deinlein U, Stephan AB, Horie T, Luo W, Xu GH, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Dohleman FG, Long SP (2009) More productive than maize in the midwest: how does Miscanthus do it? Plant Physiol 150(4):2104–2115. https://doi.org/10.1104/pp.109.139162
Giavalisco P, Li Y, Matthes A, Eckhardt A, Hubberten HM, Hesse H, Segu S, Hummel J, Kohl K, Willmitzer L (2011) Elemental formula annotation of polar and lipophilic metabolites using C-13, N-15 and S-34 isotope labelling, in combination with high- resolution mass spectrometry. Plant J 68(2):364–376. https://doi.org/10.1111/j.1365-313X.2011.04682.x
Glover JD, Reganold JP (2010) Perennial grains food security for the future. Issues Sci Technol 26(2):41–47
Glover JD, Reganold JP, Bell LW, Borevitz J, Brummer EC, Buckler ES, Cox CM, Cox TS, Crews TE, Culman SW, DeHaan LR, Eriksson D, Gill BS, Holland J, Hu F, Hulke BS, Ibrahim AMH, Jackson W, Jones SS, Murray SC, Paterson AH, Ploschuk E, Sacks EJ, Snapp S, Tao D, Van Tassel DL, Wade LJ, Wyse DL, Xu Y (2010) Increased food and ecosystem security via perennial grains. Science 328(5986):1638–1639. https://doi.org/10.1126/science.1188761
Gordon SP, Liu L, Vogel JP (2016) The genus Brachypodium as a model for perenniality and polyploidy. In: Vogel JP (ed) Genetics and genomics of Brachypodium. Springer, Cham, pp 313–325
Gruwel MLH, Rauw VL, Loewen M, Abrams SR (2001) Effects of sodium chloride on plant cells; a P-31 and Na-23 NMR system to study salt tolerance. Plant Sci 160(5):785–794. https://doi.org/10.1016/s0168-9452(00)00424-6
Hong SY, Seo PJ, Yang MS, Xiang F, Park CM (2008) Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR. BMC Plant Biol. https://doi.org/10.1186/1471-2229-8-112
Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14(12):660–668. https://doi.org/10.1016/j.tplants.2009.08.009
Katsuhara M, Kuchitsu K, Takeshige K, Tazawa M (1989) Salt stress-induced cytoplasmic acidification and vacuolar alkalization in nitellopsis-obtusa cells: in vivo p-31-nuclear magnetic-resonance study. Plant Physiol 90(3):1102–1107. https://doi.org/10.1104/pp.90.3.1102
Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59(4):609–619. https://doi.org/10.1007/s10535-015-0549-3
Kobayashi NI, Yamaji N, Yamamoto H, Okubo K, Ueno H, Costa A, Tanoi K, Matsumura H, Fujii-Kashino M, Horiuchi T, Al Nayef M, Shabala S, An G, Ma JF, Horie T (2017) OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J 91(4):657–670. https://doi.org/10.1111/tpj.13595
Krebs M, Beyhl D, Gorlich E, Al-Rasheid KAS, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. PNAS 107(7):3251–3256. https://doi.org/10.1073/pnas.0913035107
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2015) Gas chromatography mass spectrometry-based metabolite profiling in plants (vol 1, pg 387, 2006). Nat Protoc 10(9):1457–1457. https://doi.org/10.1038/nprot0915-1457a
Liu JH, Wang W, Wu H, Gong XQ, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00827
Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet. https://doi.org/10.1371/journal.pgen.1003215
McLaughlin SB, Kszos LA (2005) Development of switchgrass (Panicum virgatum) as a bioenergy feedstock in the United States. Biomass Bioenergy 28(6):515–535. https://doi.org/10.1016/j.biombioe.2004.05.006
Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol J 9(7):747–758. https://doi.org/10.1111/j.1467-7652.2010.00584.x
Plett D, Safwat G, Gilliham M, Moller IS, Roy S, Shirley N, Jacobs A, Johnson A, Tester M (2010) Improved salinity tolerance of rice through cell type-specific expression of AtHKT1;1. PLoS ONE. https://doi.org/10.1371/journal.pone.0012571
Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosyn Res 73(1–3):149–156. https://doi.org/10.1023/a:1020470224740
Queiros F, Fontes N, Silva P, Almeida D, Maeshima M, Geros H, Fidalgo F (2009) Activity of tonoplast proton pumps and Na+/H+ exchange in potato cell cultures is modulated by salt. J Exp Bot 60(4):1363–1374. https://doi.org/10.1093/jxb/erp011
Quinn LD, Straker KC, Guo J, Kim S, Thapa S, Kling G, Lee DK, Voigt TB (2015) Stress-tolerant feedstocks for sustainable bioenergy production on marginal land. Bioenergy Res 8(3):1081–1100. https://doi.org/10.1007/s12155-014-9557-y
Rea PA, Sanders D (1987) Tonoplast energization: 2 h + pumps, one membrane. Physiol Plant 71(1):131–141. https://doi.org/10.1111/j.1399-3054.1987.tb04630.x
Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37(10):1141–1146. https://doi.org/10.1038/ng1643
Sah RN, Miller RO (1992) Spontaneous reaction for acid dissolution of biological tissues in closed vessels. Anal Chem 64(2):230–233. https://doi.org/10.1021/ac00026a026
Steinwand MA, Young HA, Bragg JN, Tobias CM, Vogel JP (2013) Brachypodium sylvaticum, a model for perennial grasses: transformation and inbred line development. PLoS ONE. https://doi.org/10.1371/journal.pone.0075180
Sunarpi, Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44(6):928–938. https://doi.org/10.1111/j.1365-313X.2005.02595.x
Tilman D, Hill J, Lehman C (2006) Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314(5805):1598–1600. https://doi.org/10.1126/science.1133306
Undurraga SF, Santos MP, Paez-Valencia J, Yang HB, Hepler PK, Facanha AR, Hirschi KD, Gaxiola RA (2012) Arabidopsis sodium dependent and independent phenotypes triggered by H+-PPase up-regulation are SOS1 dependent. Plant Sci 183:96–105. https://doi.org/10.1016/j.plantsci.2011.11.011
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20. https://doi.org/10.1093/mp/ssp106
Volkov V (2015) Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00873
Wang SH, Kurepa J, Hashimoto T, Smalle JA (2011) Salt stress-induced disassembly of arabidopsis cortical microtubule arrays involves 26S proteasome-dependent degradation of SPIRAL1. Plant Cell 23(9):3412–3427. https://doi.org/10.1105/tpc.111.089920
Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proc Natl Acad Sci USA 102(44):16107–16112. https://doi.org/10.1073/pnas.0504437102
Yan J, Chen WL, Luo F, Ma HZ, Meng AP, Li XW, Zhu M, Li SS, Zhou HF, Zhu WX, Han B, Ge S, Li JQ, Sang T (2012) Variability and adaptability of Miscanthus species evaluated for energy crop domestication. GCB Bioenergy 4(1):49–60. https://doi.org/10.1111/j.1757-1707.2011.01108.x
Zhao FY, Zhang XJ, Li PH, Zhao YX, Zhang H (2006) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Mol Breed 17(4):341–353. https://doi.org/10.1007/s11032-006-9005-6
Acknowledgements
This research was supported grants from United States Department of Energy Number #DE-SC0008797 and #DE-AC02-05CH11231. XK was supported by a scholarship from the China Scholarship Council (CSC) and Nanjing Agricultural University.
Author information
Authors and Affiliations
Contributions
NS, MRW, and EdB provided research ideas and designed the experiments. NS, MRW, XK, YB, MW, IK, WDS, JPV, CMT, RT and EB participated in the implementation of the experiment, sample collection, and laboratory analysis. NS and EdB wrote the paper.
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sade, N., del Mar Rubio Wilhelmi, M., Ke, X. et al. Salt tolerance of two perennial grass Brachypodium sylvaticum accessions. Plant Mol Biol 96, 305–314 (2018). https://doi.org/10.1007/s11103-017-0696-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-017-0696-3