Effect of the fungal endophyte Epichloë bromicola on polyamines in wild barley (Hordeum brevisubulatum) under salt stress
- 122 Downloads
Background and aims
The endophytic fungus Epichloë bromicola forms mutualistic symbiotic associations with wild barley (Hordeum brevisubulatum) in the saline-alkali areas of northwestern China. E. bromicola enhances the tolerance of H. brevisubulatum to salt stress. Because plant polyamine metabolism is closely related to microbial infection and tolerance to diverse abiotic stresses, we hypothesized that in symbiotic plants polyamine modification may result from E. bromicola infection, and that improved tolerance to abiotic stress by the presence of this endophyte might be related to polyamine modification. Our focus in this study was to investigate whether E. bromicola affects polyamine metabolism in host plants under salt stress.
E. bromicola infected (E+) and endophyte free (E-) wild barley plants were subjected to NaCl treatments (0, 100, 200 and 300 mM). Dry weight, diamine putrescine (Put), triamine spermidine (Spd) and tetramine spermine (Spm) content and the content of their free, soluble conjugated and insoluble bound forms were measured after 21 d exposure to stress.
E. bromicola infection led to significant amelioration of salt stress in H. brevisubulatum. The presence of the endophyte significantly increased dry weight, spermidine and spermine content, but decreased putrescine content and the putrescine: (spermidine + spermine) ratio. E. bromicola infection also lowered the proportion of putrescine in total polyamines, but increased the proportion of spermidine and spermine in total polyamines. Furthermore, E. bromicola infection significantly increased the proportion of insoluble bound forms of polyamines, and decreased the proportion of free forms of polyamines and soluble conjugated forms of polyamines.
H. brevisubulatum salinity stress tolerance induced by E. bromicola infection correlated with enhanced conversion of putrescine to spermidine and spermine, as well as improved shift ability from free forms and soluble conjugated forms of polyamines to insoluble bound forms of polyamines.
KeywordsHordeum brevisubulatum Epichloë endophyte Salt stress Polyamines Free form polyamines Soluble conjugated form polyamines Insoluble bound form polyamines
The study was supported by National Basic Research Program of China (2014CB138702), the Natural Science Foundation of China (31372366), the Strategic Priority Research Program of Chinese Academy of Sciences (XDAXDA20100102), Program for Changjiang Scholars and Innovative Research Team in University of China (IRT17R50), Fundamental Research Funds for the Central Universities (LZUJBKY-2018-kb10), 111Project (B12002), USDA-NIFA Multistate Project W3147 and the New Jersey Agricultural Experiment Station.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
The article does not contain any studies with human participants or animals performed by any of the authors.
This study did not involve human participants, and so informed consent was not required.
- Asthir B, Spoor W, Duffus CM (2004) Involvement of polyamines, diamine oxidase and polyamine oxidase in resistance of barley to Blumeria graminis f. sp. Hordei. Euphytica 136:307–312. https://doi.org/10.1023/B:EUPH.0000032730.48474.b1 CrossRefGoogle Scholar
- Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant 104:195–202. https://doi.org/10.1034/j.1399-3054.1998.1040207.x CrossRefGoogle Scholar
- Bratton DL (1994) Polyamine inhibition of transbilayer movement of plasma membrane phospholipids in the erythrocyte ghost. J Biol Chem 269:22517–22523Google Scholar
- Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice ( Oryza sativa ) plants. Physiol Plant 116:192–199. https://doi.org/10.1034/j.1399-3054.2002.1160208.x CrossRefGoogle Scholar
- Chen TX, Simpson WR, Song QY, Chen SH, Li CJ, Ahmad RZ (2018) Identification of Epichloë endophytes associated with wild barley (Hordeum brevisubulatum) and characterisation of their alkaloid biosynthesis. New Zeal J Agr Res. https://doi.org/10.1080/00288233.2018.1461658
- Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45(2):84–93. https://doi.org/10.1016/j.fgb.2007.07.013 CrossRefGoogle Scholar
- Fiscaletti D, Angeli D, Tarozzi L, Barozzi GS (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35:2015–2036. https://doi.org/10.1016/j.ijheatmasstransfer.2012.11.039 CrossRefGoogle Scholar
- Ghachtouli NE, Martin-Tanguy J, Paynot M, Gianinazzi S (1996) First-report of the inhibition of arbuscular mycorrhizal infection of Pisum sativum by specific and irreversible inhibition of polyamine biosynthesis or by gibberellic acid treatment. FEBS Lett 385:189–192. https://doi.org/10.1016/0014-5793(96)00379-1 CrossRefGoogle Scholar
- Greenland AJ, Lewis DH (1984) Amines in barley leaves infected by brown rust and their possible relevance to formation of 'green islands'. New Phytol 96:283–291. https://doi.org/10.1111/j.1469-8137.1984.tb03565.x CrossRefGoogle Scholar
- Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596. https://doi.org/10.1155/2014/701596
- Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722. https://doi.org/10.1093/pcp/pch083 CrossRefGoogle Scholar
- Kuznetsov VV, Shevyakova NI (2007) Polyamines and stress tolerance of plants. Plant Stress 1:50–71Google Scholar
- Ma M, Christensen MJ, Nan Z (2015) Effects of the endophyte Epichloë festucae var. lolii of perennial ryegrass ( Lolium perenne ) on indicators of oxidative stress from pathogenic fungi during seed germination and seedling growth. Eur J Plant Pathol 141:571–583. https://doi.org/10.1007/s10658-014-0563-x CrossRefGoogle Scholar
- Margosiak SA, Dharma A, Brucecarver MR, Gonzales AP, Louie D, Kuehn GD (1990) Identification of the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase as a substrate for transglutaminase in Medicago sativa L. (alfalfa). Plant Physiol 92:88–96. https://doi.org/10.1104/pp.92.1.88 CrossRefGoogle Scholar
- Martin-Tanguy J (1997) Conjugated polyamines and reproductive development: biochemical, molecular and physiological approaches. Physiol Plant 100:675–688. https://doi.org/10.1111/j.1399-3054.1997.tb03074.x CrossRefGoogle Scholar
- Monnet F, Vaillant N, Hitmi A, Coudret A, Sallanon H (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiol Plant 113:557–563. https://doi.org/10.1034/j.1399-3054.2001.1130415.x CrossRefGoogle Scholar
- Omar MNA, Osman MEH, Kasim WA, El-Daim IAA (2009) Improvement of salt tolerance mechanisms of barley cultivated under salt stress using Azospirillum brasilense. In: Ashraf M, Ozturk M, Athar HR (eds) Salinity and water stress: improving crop efficiency. Springer, Dordrecht, pp 133–147CrossRefGoogle Scholar
- Pál M, Kovács V, Vida G, Szalai G, Janda T (2011) Changes in salicylic acid and polyamine contents following powdery mildew infection of near-isogenic thatcher-based wheat lines carrying different Lr genes. Acta Biol Szeged 55:139–141Google Scholar
- Prakash L, Prathapasenan G (1988) Effect of NaCl salinity and putrescine on shoot growth, tissue ion concentration and yield of rice (Oryza sativa L. var. GR-3). J Agron Crop Sci 160:325–334. https://doi.org/10.1111/j.1439-037X.1988.tb00630.x CrossRefGoogle Scholar
- Rozpądek P, Rozpadek P, Wezowicz K, Nosek M, Wazny R, Tokarz K, Lembicz M, Miszalski Z, Turnau K (2015) The fungal endophyte Epichloë typhina improves photosynthesis efficiency of its host orchard grass (Dactylis glomerata). Planta 242:1025–1035. https://doi.org/10.1007/s00425-015-2337-x CrossRefGoogle Scholar
- Santa-Cruz A, Acosta M, Pérez-Alfocea F, Bolarin MC (1997) Changes in free polyamine levels induced by salt stress in leaves of cultivated and wild tomato species. Physiol Plant 101:341–346. https://doi.org/10.1111/j.1399-3054.1997.tb01006.x CrossRefGoogle Scholar
- Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O'Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, Leistner E, Leuchtmann A, Li C, Liu JG, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z (2013) Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 9:e1003323. https://doi.org/10.1371/journal.pgen.1003323 CrossRefGoogle Scholar
- Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665. https://doi.org/10.1104/pp.106.082388 CrossRefGoogle Scholar
- Song ML (2015) Mechanisms of salt tolerance improved by Epichloë endophyte in wild barley. Dissertation: Lanzhou UniversityGoogle Scholar
- Walters DR, Wylie MA (1986) Polyamines in discrete regions of barley leaves infected with the powdery mildew fungus, Erysiphe graminis. Physiol Plant 67:630–633. https://doi.org/10.1111/j.1399-3054.1986.tb05068.x CrossRefGoogle Scholar
- Wang CM, Xia ZR, Wu GQ, Yuan HJ, Wang XR, Li JH, Tian FP, Zhang Q, Zhu XQ, He JJ, Kumar T, Wang XL, Zhang JL (2016) The coordinated regulation of Na+ and K+ in Hordeum brevisubulatum responding to time of salt stress. Plant Sci 252:358–366. https://doi.org/10.1016/j.plantsci.2016.08.009 CrossRefGoogle Scholar
- Xia C, Li NN, Zhang XX, Feng Y, Christensen MJ, Nan ZB (2016) An Epichloë endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol 22:26–34. https://doi.org/10.1016/j.funeco.2016.04.002 CrossRefGoogle Scholar
- Zepeda-Jazo I, Velarde-Buendia AM, Enriquez-Figueroa R, Bose J, Shabala S, Muniz-Murguia J, Pottosin II (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 157:2167–2180. https://doi.org/10.1104/pp.111.179671 CrossRefGoogle Scholar