Abstract
This study aimed to investigate the influence of the fungus Trichoderma asperellum on photosynthesis and nitrogen metabolism in maize seedlings of different genotypes, subjected to saline–alkaline stress. Saline–alkaline tolerant and sensitive varieties, Jiangyu 417 and Xianyu 335 (XY335), respectively, were grown in naturally saline–alkaline soil (pH 9.30) in 5-inch pots. Root and leaf samples were collected when seedlings had three heart-shaped leaves and the fourth leaf developing. Meadow soil (pH 8.23) was used as a positive control. Saline–alkaline stress remarkably increased NH4+ content and caused ammonia toxicity, weakened the ammonium assimilation process, and reduced photosynthesis in maize seedlings. Our results show that T. asperellum alleviated these effects to a certain degree, especially in XY335. The application of T. asperellum likely improved the content of photosynthetic pigments, enhanced the photochemical activity of the photosystem II reaction center, increased the activities of ATP enzymes in the chloroplasts, reduced the non-stomatal limitation of photosynthesis owing to saline–alkaline stress, and promoted photosynthesis to provide more raw materials and energy for nitrogen metabolism, thereby improving the activity of nitrogen metabolism and the capacity for material production in maize seedlings. By coordinating the synergistic effect of glutamate dehydrogenase, glutamine synthetase/glutamate synthase, and transamination, T. asperellum promoted the assimilation of excessively accumulated ammonia, maintained the balance of NH4+ and the enzymes related to its metabolism, and subsequently alleviated ammonia toxicity and negative changes in nitrogen metabolism resulting from saline–alkaline stress. Thus, the application of T. asperellum alleviated damage to chloroplasts and thylakoid membranes, and improved nitrogen metabolism, thereby promoting seedling growth. The concentration of 1 × 109 spores L−1 was found to be the most effective and economical treatment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbasi GH, Akhtar J, Ahmad R, Jamil M, Anwar- Ul-Haq M, Ali S, Ijaz M (2015) Potassium application mitigates salt stress differentially at different growth stages in tolerant and sensitive maize hybrids. Plant Growth Regul 76:111–125. https://doi.org/10.1007/s10725-015-0050-1
Abbasi GH, Akhtar J, Anwar-Ul-Haq M, Malik W, Ali S, Chen ZH, Zhang GP (2016) Morphophys-iological and micrographic characterrization of maize hybrids under nacl and cd stress. Plant Growth Regul 75:1–8. https://doi.org/10.1007/s10725-014-9936-6
An YM, Song LL, Liu YR, Shu YJ, Guo CH (2016). De novotranscriptional analysis of alfalfa in response to saline-alkaline stress. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00931
Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in beta vulgaris. Plant Physiol 24(1):1
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brotman Y, Landau U, Cuadrosinostroza A, Tohge T, Fernie AR, Chet I, Viterbo A, Willmtizer I (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. Plos Pathogens 9:130–139. https://doi.org/10.1371/journal.ppat.1003221
Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid 1. Commun Soil Sci Plant 6:71–80. https://doi.org/10.1080/00103627509366547
Chine HF, Kao CH (2000) Accumulation of ammonium in rice leaves in response to excess cadmium. Plant Sci 156:111–115. https://doi.org/10.1016/S0168-9452(00)00234-X
Demmig-Adams B, Adams WW (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470. https://doi.org/10.1007/bf00620064
Dickmann DI (1971) Chlorophyll, ribulose-1,5-diphosphate carboxylase, and Hill reaction activity in developing leaves of populus deltoides. Plant Physiol 48:143–145. https://doi.org/10.1104/pp.48.2.143
Fu J, Liu Z, Li Z, Wang Y, Yang K (2017) Alleviation of the effects of saline-alkaline stress on maize seedlings by regulation of active oxygen metabolism by Trichoderma asperellum. PLoS ONE 12:e0179617. https://doi.org/10.1371/journal.pone.0179617
Gangwar S. Singh VP (2011) Indole acetic acid differently changes growth and nitrogen metabolism in Pisum sativum L. seedlings under chromium (VI) phytotoxicity: implication of oxidative stress. Sci Hortic 29:321–328. https://doi.org/10.1016/j.scienta
Guler NS, Pehlivan N, Karaoglu SA, Guzel S, Bozdeveci A (2016) Trichoderma atroviride ID20G inoculation ameliorates drought stress-induced damages by improving antioxidant defence in maize seedlings. Acta Physiol Plant 38(6):1–3. https://doi.org/10.1007/s11738-016-2153-3
Juan M, Rivero RM, Romero L, Ruiz JM (2005) Evaluation of some nutritional and biochemical indicators in selecting salt-resistant tomato cultivars. Environ Exp Bot 54:193–201. https://doi.org/10.1016/j.envexpbot
Krom MD (1980) Spectrophotometric determination of ammonia: a study of a modified Berthelot reaction using salicy-late and dichlor-oisocyanurate. Analyst 105:305–316. https://doi.org/10.1039/an9800500305
Liang CG, Chen LP, Wang Y, Liu J, Xu GL, Li T (2011) High temperature at grain-filling stage affects nitrogen metabolism enzyme activities in grains and grain nutritional quality in rice. Rice Sci 18:210–216
Lutts S, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398. https://doi.org/10.1006/anbo.1996.0134
McCarty RE (2005) ATP synthase of chloroplast thylakoid membranes: a more in depth eharacterization of its ATPase activity. J Bioenerg Biomembr. https://doi.org/10.1007/s10863-005-8640-7
Mccarty RE, Racker E (1968) Partial resolution of the enzymes catalyzing photophosphorylation. 3.activation of adenosine triphosphatase and 32p-labeled orthophosphate-adeno-sine triphosphate exchange in chloroplasts. J Biol Chem 243(1):129
Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotechnol 98:8777–8796. https://doi.org/10.1007/s00253-014-6020-0
Pandey V, Ansari MW, Tula S, Yadav S, Sahoo RK, Shukla N (2016) Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 243:1251–1264. https://doi.org/10.1007/s00425-016-2482-x
Peng YQ, Xie T, Zhou F, Wan HJ, Zhang CY, Zhai RT, Zheng QS, Zheng CF, LIu ZP (2012) Response of plant growth and photosynthetic characteristics in Suaeda glauca and Atriplex triangularis seedlings to different concentrations of salt treatmengts. Acta Prataculturae Sin 21:64–74
Rozema J, Flowers T (2008) Crops for a salinized world. Science 322:1478–1480
Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Ríos JJ, Blasco B, Rosales M, Melgarejo R, Romero L, Ruiz JM (2011) Ammonia production and assimilation: its importance as a tolerance mechanism during moderate water deficit in tomato plants. J Plant Physiol 168:816–823. https://doi.org/10.1016/j.jplph.2010.11.018
Shi XB, Wei JM, Shen YK (2001) Effeets of sequential deletions of residues from the N-or Cterminus on the function of subunit of the chioroplast ATP synthase. Bioehemistry 40:10825–10831
Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Phytopathology 48:21–43. https://doi.org/10.1146/annurev-phyto-073009-114450
Song J, Feng G, Tian CY, Zhang FS (2006) Osmotic adjustment traits of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum in field or controlled conditions. Plant Sci 170:113–119. https://doi.org/10.1016/j.plantsci.2005.08.004
Soussi M, Lluch C, Ocana A, Norero AL (1999) Comparative study of nitrogen fixation and carbon metabolism in two chick-pea (Cicer arietinum L.) cultivars under salt stress. J Exp Bot 50:1701–1708. https://doi.org/10.1093/jexbot/50.340.1701
Teh CY, Mahmood M, Shaharuddin NA, Chai LH (2015) In vitro rice shoot apices as simple model to study the effect of nacl and the potential of exogenous proline and glutathione in mitigating salinity stress. Plant Growth Regul 75:771–781. https://doi.org/10.1007/s10725-014-9980-2
Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol andplant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48. https://doi.org/10.1111/j.1574-6968.2010.01910.x
Wang XP, Geng SJ, Ri YJ, Cao DH, Liu J, Shi DC, Yang CW (2011) Physiological responses and adaptive strategies of tomato plants to salt and alkali stresses. Sci Hortic 130:248–255. https://doi.org/10.1016/j.scienta.2011.07.006
Wu HS, Yin XM, Zhu YY, Guo SW, Wu CL, Lu YL, Shen QR (2007) Nitrogen metabolism disorder in watermelon leaf caused by fusaric acid. Physiol Mol Plant Pathol 71:69–77. https://doi.org/10.1016/j.pmpp
Wu X, Liu C, Qu CX, Huang H, Liu XQ, Chen L, Hong FS (2008) Effects of lead on activities of photochemical reaction and key enzymes of carbon assimilation in spinach chloroplast. Biol Trace Elem Res 126:269–279. https://doi.org/10.1007/s12011-008-8196-6
Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070
Zhang J, Zhang Y, Du Y, Chen S, Tang H (2011) Dynamic Metabonomic Responses of Tobacco (Nicotiana tabacum) Plants to Salt Stress. J Proteome Res 10:1904–1914. https://doi.org/10.1021/pr101140n
Zhang Y, Hu XH, Shi Y, Zou ZR, Yan F, Zhao YY, Zhang H, Zhao JZ (2013) Beneficial role of exogenous spermidine on nitrogen metabolism in tomato seedlings exposed to saline-alkaline stress. J Am Soc Hortic Sci 138:38–49
Zhang S, Gan Y, Xu B (2016) Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front Plant Sci 7(868):1405. https://doi.org/10.3389/fpls.2016.01405
Acknowledgements
This work was supported by grants from National science and technology support plan of china (2013BAD07B01); Chinese National science and technology support plan (2015BAD23B05-04); Heilongjiang Bayi Agricultural university graduate student innovation fund projects (YJSCX2016-Z01)。Thanks for forestry college of northeast forestry university “Trichoderma research team” to provide “Dedicated Trichoderma of maize".
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Fu, J., Wang, Yf., Liu, Zh. et al. Trichoderma asperellum alleviates the effects of saline–alkaline stress on maize seedlings via the regulation of photosynthesis and nitrogen metabolism. Plant Growth Regul 85, 363–374 (2018). https://doi.org/10.1007/s10725-018-0386-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-018-0386-4