Abstract
Global soil salinization is becoming increasingly severe. Many excellent garden trees cannot be planted in coastal or saline-alkali parks. Traditional methods such as freshwater washing and deep tilling consume substantial financial and human resources; hence, it is a promising strategy to search for a biological alternative. Seventy-eight fungal endophytic strains were isolated from the roots of alive Acer buergerianum (trident maple). Through a salt-resistance test, a strain was found to improve the salt tolerance of the seedlings. We explored the mechanism of improvement of salt resistance of the seedlings with this isolate by determining the levels of compounds and enzyme activities associated with salt resistance of the seedlings. ACS53 was identified as a species of the genus Cylindrocarpon by morphological and molecular evaluation. This strain substantially increased the contents of abscisic acid (ABA), proline, and soluble sugar and the activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), which are related to stress tolerance, in seedlings under salt stress. The isolate also showed an ability to secrete abundant extracellular ABA, which may trigger salt tolerance of the seedlings. Biological methods are considered a potential strategy to cope with saline land. In this study, strain ACS53 belonging to the genus Cylindrocarpon was found to substantially improve the salt resistance of trident maple seedlings under salt stress. This may provide a potential sustainable method against salinization. It may also be helpful to better understand how a fungal endophyte improves the salt resistance of host plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during the current study are available from the corresponding author upon reasonable request.
References
Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18. https://doi.org/10.3390/agronomy7010018
Acuña JJ, Campos M, de la Luz MM, Jaisi DP, Jorquera MA (2019) ACCD-producing rhizobacteria from an Andean Altiplano native plant (Parastrephia quadrangularis) and their potential to alleviate salt stress in wheat seedlings. Appl Soil Ecol 136:184–190. https://doi.org/10.1016/j.apsoil.2019.01.005
Ait-El-Mokhtar M, Laouane RB, Anli M, Boutasknit A, Wahbi S, Meddich A (2019) Use of mycorrhizal fungi in improving tolerance of the date palm (Phoenix dactylifera L.) seedlings to salt stress. Sci Hortic 253:429–438. https://doi.org/10.1016/j.scienta.2019.04.066
Akbari G, Sanavy SA, Yousefzadeh S (2007) Effect of auxin and salt stress (NaCl) on seed germination of wheat cultivars (Triticum aestivum L.). Pakistan J Biol Sci 10:2557–2561. https://doi.org/10.3923/pjbs.2007.2557.2561
Amjad M, Akhtar J, Anwar-ul-Haq M, Yang A, Akhtar SS, Jacobsen SE (2014) Integrating role of ethylene and ABA in tomato plants adaptation to salt stress. Sci Hortic 172:109–116. https://doi.org/10.1016/j.scienta.2014.03.024
Anam GB, Reddy MS, Ahn YH (2019) Characterization of Trichoderma asperellum RM-28 for its sodic/saline-alkali tolerance and plant growth promoting activities to alleviate toxicity of red mud. Sci Total Environ 662:462–469. https://doi.org/10.1016/j.scitotenv.2019.01.279
Aragno M (1981) Responses of microorganisms to temperature. In: Lange OL, Nobel PS, Osmond CB, Ziegle H. (ed) Physiological plant ecology I. Encyclopedia of plant physiology, vol. 12/A. Springer, Heidelberg, pp 339–369. https://doi.org/10.1007/978-3-642-68090-8_12
Aroca R, Ruiz-Lozano JM, Zamarreño ÁM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55. https://doi.org/10.1016/j.jplph.2012.08.020
Ashraf M, Foolad MR (2005) Pre-sowing seed treatment-a shotgun approach to improving germination, plant growth and crop yield under saline and non-saline conditions. Adv Agron 88:223–271. https://doi.org/10.1016/S0065-2113(05)88006-X
Atia A, Barhoumi Z, Debez A, Hkiri S, Abdelly C, Smaoui A, Haouari CC, Gouia H (2018) Plant hormones: potent targets for engineering salinity tolerance in plants. In: Kumar V, Wani S, Suprasanna P, Tran LS (eds) Salinity responses and tolerance in plants, vol 1. Springer Cham, pp 159–184. https://doi.org/10.1007/978-3-319-75671-4_6
Aung K, Jiang Y, He SY (2018) The role of water in plant-microbe interactions. Plant J 93:771–780. https://doi.org/10.1111/tpj.13795
Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fert Soils 45:405–413. https://doi.org/10.1007/s00374-008-0344-9
Batnini M, Fernández Del-Saz N, Fullana-Pericàs M, Palma F, Haddoudi I, Mrabet M, Ribas-Carbo M, Mhadhbi H (2020) The alternative oxidase pathway is involved in optimizing photosynthesis in Medicago truncatula infected by Fusarium oxysporum and Rhizoctonia solani. Physiol Plantarum 169:600–611. https://doi.org/10.1111/ppl.13080
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068
Bhardwaj S, Kumar P (2020) Salinity stress, its physiological response and mitigating effects of microbial bio inoculants and organic compounds. J Pharmacogn Phytochem 9:1297–1303. https://doi.org/10.22271/phyto.2020.v9.i4r.11925
Bukharina IL, Islamova NA (2020) Metal resistance and tolerance to temperature stress of plants inoculated with endophyte Cylindrocarpon magnusianum wollenw. Agrobiodivers Improv Nutr, Health Life Qual 4 https://agrobiodiversity.uniag.skscientificpapers/article/view/318
Bukharina IL, Islamova NA, Lebedeva MA (2021) Effect of inoculating the root system of plants with endophyte Cylindrocarpon magnusianum on plant performance when exposed to heavy metal salts. Russ Agric Sci 47:42–47. https://doi.org/10.3103/S1068367421010067
Bukharina IL, Islamova NA, Zhavad AF, Lebedeva MA, Shashov LO (2019) The influence of the inoculum Cylindrocarpon magnusianum on the formation of adaptive responses of plants to stress factors. Agrarnaya Rossiya 12:26–32. https://doi.org/10.30906/1999-5636-2019-12-26-32
Cabral A, Groenewald JZ, Rego C, Oliveira H, Crous PW (2012) Cylindrocarpon root rot: multi-gene analysis reveals novel species within the Ilyonectria radicicola species complex. Mycol Prog 11:655–688. https://doi.org/10.1007/s11557-011-0777-7
Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2–9. https://doi.org/10.2307/1943154
Chaverri P, Salgado C, Hirooka Y, Rossman AY, Samuels GJ (2011) Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon-like anamorphs. Stud Mycol 68:57–78. https://doi.org/10.3114/sim.2011.68.03
Chen G, Zheng D, Feng N, Zhou H, Mu D, Zhao L, Shen X, Rao G, Meng F, Huang A (2022) Physiological mechanisms of ABA-induced salinity tolerance in leaves and roots of rice. Sci Rep 12:1–26. https://doi.org/10.1038/s41598-022-11408-0
Cho K, Toler H, Lee J, Ownley B, Stutz JC, Moore JL, Augé RM (2006) Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. J Plant Physiol 163:517–528. https://doi.org/10.1016/j.jplph.2005.05.003
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75. https://doi.org/10.1242/jeb.089938
Costa SF, Martins D, Agacka-Mołdoch M, Czubacka A, Sousa Araújo SD (2018) Strategies to alleviate salinity stress in plants. In: Kumar V, Wani SH, Suprasanna P, LSP T (eds) Salinity responses and tolerance in plants. Springer Switzerland, pp 307–337. https://doi.org/10.1007/978-3-319-75671-4_12
Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428. https://doi.org/10.1093/jxb/ers033
Dunlap J, Binzel M (1996) NaCl reduces indole-3-acetic acid levels in the roots of tomato plants independent of stressinduced abscisic acid. Plant Physiol 112:379–384. https://doi.org/10.1104/pp.112.1.379
Eid AM, Salim SS, Hassan SED, Ismail MA, Fouda A (2019) Role of endophytes in plant health and abiotic stress management. In: Kumae V, Prasad R, Kumar M, Choudhary DK (eds) Microbiome in plant health and disease. Springer Singapore, pp 119–144. https://doi.org/10.1007/978-981-13-8495-0_6
Eisenhauer N, Lanoue A, Strecker T Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep 7:4641. https://doi.org/10.1038/srep44641
Etesami H, Glick BR (2020) Halotolerant plant growth-promoting bacteria: prospects for alleviating salinity stress in plants. Environ Exp Bot 178:104124. https://doi.org/10.1016/j.envexpbot.2020.104124
Fang R, Lin J, Yao S Wang Y, Wang J, Zhou C, Wang H, Xiao M (2013) Promotion of plant growth, biological control and induced systemic resistance in maize by Pseudomonas aurantiaca JD37. Ann Microbiol 63:1177–1185. https://doi.org/10.1007/s13213-012-0576-7
Farh MEA, Kim YJ, Yang DC (2018) Cylindrocarpon destructans/Ilyonectria radicicola-species complex: causative agent of ginseng root-rot disease and rusty symptoms. J Ginseng Res 42:9–15. https://doi.org/10.1016/j.jgr.2017.01.004
Forni C, Duca D, Glick BR (2017) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 410:335–356. https://doi.org/10.1007/s11104-016-3007-x
Galinski EA, Trüper HG (1994) Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol Rev 15:95–108. https://doi.org/10.1111/j.1574-6976.1994.tb00128.x
García-Gómez P, Bahaji A, Gámez-Arcas S, Muñoz FJ, Sánchez-López ÁM, Almagro G, Baroja-Fernández B, Ameztoy K, Diego ND, Ugena L (2020) Volatiles from the fungal phytopathogen Penicillium aurantiogriseum modulate root metabolism and architecture through proteome resetting. Plant Cell Environ 43:2551–2570. https://doi.org/10.1111/pce.13817
Gómez-Cadenas A, Arbona V, Jacas J, Primo-Millo E, Talon M (2002) Abscisic acid reduces leaf abscission and increases salt tolerance in citrus plants. J Plant Growth Regul 21:234–240. https://doi.org/10.1007/s00344-002-0013-4
Guo G, Araya K, Jia H, Zhang Z, Ohomiya K, Matsuda J (2006) Improvement of salt-affected soils, part 1: interception of capillarity. Biosyst Eng 94:139–150. https://doi.org/10.1016/j.biosystemseng.2006.01.012
Gupta S, Schillaci M, Walker R, Smith P, Watt M, Roessner U (2021) Alleviation of salinity stress in plants by endophytic plant-fungal symbiosis: current knowledge, perspectives and future directions. Plant Soil 461:219–244. https://doi.org/10.1007/s11104-020-04618-w
Hao S, Wang Y, Yan Y, Liu Y, Wang J, Chen SA (2021) Review on plant responses to salt stress and their mechanisms of salt resistance. Horticulturae 7:132. https://doi.org/10.3390/horticulturae7060132
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P, Azooz MM, MNV P (eds) Ecophysiology and responses of plants under salt stress. Springer, USA, pp 25–87. https://doi.org/10.1007/978-1-4614-4747-4_2
Hernández-Canseco J, Bautista-Cruz A, Sánchez-Mendoza S, Aquino-Bolaños T, Sánchez-Medina PS (2022) Plant growth-promoting halobacteria and their ability to protect crops from abiotic stress: an eco-friendly alternative for saline soils. Agronomy 12:804. https://doi.org/10.3390/agronomy12040804
Hidangmayum A, Dwivedi P (2018) Plant responses to Trichoderma spp. and their tolerance to abiotic stresses: a review. J Pharmacogn Phytochem 7:758–766
Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5:726–734
Jones MM, Rawson HM (1979) Influence of rate of development of leaf water deficits upon photosynthesis, leaf conductance, water use efficiency, and osmotic potential in sorghum. Physiol Plantarum 45:103–111. https://doi.org/10.1111/j.1399-3054.1979.tb01672.x
Jones MM, Turner NC (1978) Osmotic adjustment in leaves of sorghum in response to water deficits. Plant Physiol 61:122–126. https://doi.org/10.1104/pp.61.1.122
Kamaruzzaman M, Wang Z, Wu M, Yang L, Han Y, Li G, Zhang J (2021) Promotion of tomato growth by the volatiles produced by the hypovirulent strain QT5-19 of the plant gray mold fungus Botrytis cinerea. Microbiol Res 247:126731. https://doi.org/10.1016/j.micres.2021.126731
Kaya C, Tuna AL, Yokas I (2009) The role of plant hormones in plants under salinity stress. In: Ashraf M, Ozturk M, Athar HR (eds) Salinity and water stress: improving crop efficiency. Springer, Berlin, pp 45–50. https://doi.org/10.1007/978-1-4020-9065-3_5
Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP (2020) Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol 11:1216. https://doi.org/10.3389/fmicb.2020.01216
Kumar A, Verma JP (2018) Does plant-microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52. https://doi.org/10.1016/j.micres.2017.11.004
Kumawat KC, Nagpal S, Sharma P (2022) Potential of plant growth-promoting rhizobacteria-plant interactions in mitigating salt stress for sustainable agriculture: a review. Pedosphere 32:223–245. https://doi.org/10.1016/S1002-0160(21)60070-X
Li L, Li L, Wang X, Zhu P, Wu H, Qi S (2017) Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Plant Physiol Bioch 119:211–223. https://doi.org/10.1016/j.plaphy.2017.08.029
Li XJ, Yang MF, Chen H, Qu LQ, Chen F, Shen SH (2010) Abscisic acid pretreatment enhances salt tolerance of rice seedlings: proteomic evidence. BBA-Proteins Proteom 1804:929–940. https://doi.org/10.1016/j.bbapap.2010.01.004
Li Y, Yang J, Zhou X, Zhao W, Jian Z (2015) Isolation and identifcation of a 10-deacetyl baccatin-III-producing endophyte from Taxus wallichiana. Appl Biochem Biotechnol 175:2224–2231. https://doi.org/10.1007/s12010-014-1422-0
Lu MY (1982) Study on the method for determining soil salt content. Chin J Soil Sci 02:36–39
Lubnaa AS, Hamayun M, Khan AL, Waqas M, Khan MA, Jan R, Lee I, Hussain A (2018) Salt tolerance of Glycine max. L induced by endophytic fungus Aspergillus flavus CSH1, via regulating its endogenous hormones and antioxidative system. Plant Physiol Bioch 12:13–23. https://doi.org/10.1016/j.plaphy.2018.05.007
Ma Y, Dias MC, Freitas H (2020) Drought and salinity stress responses and microbe-induced tolerance in plants. Front Plant Sci 11:591911. https://doi.org/10.3389/fpls.2020.591911
Maas EV (1993) Plant growth response to salt stress. In: Lieth H, Masoom A (eds) Towards the rational use of high salinity tolerant plants. Springer, Holland, pp 279–291. https://doi.org/10.1007/978-94-011-1858-3_31
Maggio A, Barbieri G, Raimondi G, De Pascale S (2010) Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J Plant Growth Regul 29:63–72. https://doi.org/10.1007/s00344-009-9114-7
Malgioglio G, Rizzo GF, Nigro S, du Prey VL, Herforth-Rahmé J, Catara V, Branca F (2022) Plant-microbe interaction in sustainable agriculture: the factors that may influence the efficacy of PGPM application. Sustainability 14:2253. https://doi.org/10.3390/su14042253
Mastouri F, Björkman T, Harman GE (2012) Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol Plant Microbe In 25:1264–1271. https://doi.org/10.1094/MPMI-09-11-0240
Miransari M (2017) Arbuscular mycorrhizal fungi and soil salinity. In: Johnson NC, Gehring C, Jansa J (eds) Mycorrhizal Mediation of Soil. Elsevier, Netherlands, pp 263–277. https://doi.org/10.1016/B978-0-12-804312-7.00015-2
Murali M, Naziya B, Ansari MA, Alomary MN, AIYahya S, Almatroudi A, Thriveni MC, Gowtham HG, Singh SB, Aiyaz M (2021) Bioprospecting of rhizosphere-resident fungi: their role and importance in sustainable agriculture. J Fungi 7:314. https://doi.org/10.3390/jof7040314
Naamala J, Smith DL (2021) Microbial derived compounds are a promising approach to mitigating salinity stress in agricultural crops. Front Microbiol 19:765320. https://doi.org/10.3389/fmicb.2021.765320
Narsing Rao MP, Dong ZY, Xiao M, Li WJ (2019) Effect of salt stress on plants and role of microbes in promoting plant growth under salt stress. In: Giri B, Varma A (eds) Microorganisms in saline environments: strategies and functions. Springer, Switzerland, pp 423–435. https://doi.org/10.1007/978-3-030-18975-4_18
Nazari M, Smith DL (2020) A PGPR-produced bacteriocin for sustainable agriculture: a review of thuricin 17 characteristics and applications. Front Plant Sci 11:916. https://doi.org/10.3389/fpls.2020.00916
Nelson PG, May G (2017) Coevolution between mutualists and parasites in symbiotic communities may lead to the evolution of lower virulence. Am Nat 190:803–817 http://orcid.org/0000-0003-4453-9895
Olexa MT, Freeman TE (1978) A gall disease of red mangrove caused by Cylindrocarpon didymum. Plant Dis Rep 62:283–286
Ondrasek G, Rathod S, Manohara KK, Gireesh C, Anantha MS, Sakhare AS, Parmar B, Yadav BK, Bandumula N, Raihan F (2022) Salt stress in plants and mitigation approaches. Plants 11:717. https://doi.org/10.3390/plants11060717
Pandey V, Ansari MW, Tula S, Yadav S, Sahoo RK, Shukla N, Bains G, Badal S, Chandra S, Gaur AK (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
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut R 22:4056–4075. https://doi.org/10.1007/s11356-014-3739-1
Petit E, Gubler WD (2005) Characterization of Cylindrocarpon species, the cause of black foot disease of grapevine in California. Plant Dis 89:1051–1059. https://doi.org/10.1094/PD-89-1051
Pollastri S, Savvides A, Pesando M, Lumini E, Volpe MG, Ozudogru EA, Faccio A, De Cunzo F, Michelozzi M, Lambardi M (2018) Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta 247:573–585. https://doi.org/10.1007/s00425-017-2808-3
Posada LF, Ramírez M, Ochoa-Gómez N, Cuellar-Gaviria TZ, Argel-Roldan LE, Ramírez CA, Villegas-Escobar V (2016) Bioprospecting of aerobic endospore-forming bacteria with biotechnological potential for growth promotion of banana plants. Scientia Hortic 212:81–90. https://doi.org/10.1016/j.scienta.2016.09.040
Qadir M, Schubert S, Badia D, Sharma BR, Qureshi AS, Murtaza G (2007) Amelioration and nutrient management strategies for sodic and alkali soils. CAB Rev. Perspect Agric Vet Sci Nutr Nat Resour 21:1–13. https://doi.org/10.1079/PAVSNNR20072021
Qin S, Feng WW, Wang TT, Ding P, Xing K, Jiang JH (2017) Plant growth-promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp. KLBMP 5084 isolated from halophyte Limonium sinense. Plant Soil 416:117–132. https://doi.org/10.1007/s11104-017-3192-2
Ratzke C, Gore J (2018) Modifying and reacting to the environmental pH can drive bacterial interactions. PLoS Biol 16:e2004248. https://doi.org/10.1371/journal.pbio.2004248
Rawat L, Singh Y, Shukla N, Kumar J (2011) Alleviation of the adverse effects of salinity stress in wheat (Triticum aestivum L.) by seed biopriming with salinity tolerant isolates of Trichoderma harzianum. Plant Soil 347:387. https://doi.org/10.1007/s11104-011-0858-z
Rodríguez-Llorente ID, Pajuelo E, Navarro-Torre S, Mesa-Marín J, Caviedes MA (2019) Bacterial endophytes from halophytes: how do they help plants to alleviate salt stress? In: Kumar M, Etesami H, Kumar V (eds) Saline soil-based agriculture by halotolerant microorganisms. Springer, Singapore, pp 147–160. https://doi.org/10.1007/978-981-13-8335-9_6
Ryu H, Cho YG (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155
Sade N, Galkin E, Moshelion M (2015) Measuring Arabidopsis, tomato and barley leaf relative water content (RWC). Bio-protocol 5:e1451–e1451. https://doi.org/10.21769/BioProtoc.1451
Sánchez-López ÁM, Baslam M, De Diego N, Muñoz FJ, Bahaji A, Almagro G, Ricarte-Bermejo A, García-Gómez P, Li J, Humplík JF (2016) Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. Plant Cell Environ 39:2592–2608. https://doi.org/10.1111/pce.12759
Saxena B, Shukla K, Giri B (2017) Arbuscular mycorrhizal fungi and tolerance of salt stress in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Switzerland, pp 67–97. https://doi.org/10.1007/978-981-10-4115-0_4
Sengupta N (2002) Traditional vs modern practices in salinity control. Econ Polit Wkly 37:1247–1254
Shilev S (2020) Plant-growth-promoting bacteria mitigating soil salinity stress in plants. Appl Sci 10:7326. https://doi.org/10.3390/app10207326
Singh A (2021) Soil salinization management for sustainable development: a review. J Environ Manage 277:111383. https://doi.org/10.1016/j.jenvman.2020.111383
Sripinyowanich S, Klomsakul P, Boonburapong B, Bangyeekhun T, Asami T, Hongya GH, Buaboocha T, Chadchawan S (2013) Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): the role of OsP5CS1 and OsP5CR gene expression during salt stress. Environ Exp Bot 86:94–105. https://doi.org/10.1016/j.envexpbot.2010.01.009
Subramanian S, Ricci E, Souleimanov A, Smith DL (2016a) A proteomic approach to lipo-chitooligosaccharide and thuricin 17 effects on soybean germination unstressed and salt stress. PLoS One 11:e0160660. https://doi.org/10.1371/journal.pone.0160660
Subramanian S, Souleimanov A, Smith DL (2016b) Proteomic studies on the effects of lipo-chitooligosaccharide and thuricin 17 under unstressed and salt stressed conditions in Arabidopsis thaliana. Front Plant Sci 7:1314
Sunita K, Mishra I, Mishra J, Prakash J, Arora NK (2020) Secondary metabolites from halotolerant plant growth promoting rhizobacteria for ameliorating salinity stress in plants. Front Microbiol 11:567768. https://doi.org/10.3389/fmicb.2020.567768
Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK (2011) Additive effects of Na+ and Cl– ions on barley growth under salinity stress. J Exp Bot 62:2189–2203. https://doi.org/10.1093/jxb/erq422
Tsavkelova EA, Cherdyntseva TA, Klimova SY, Shestakov AI, Botina SG, Netrusov AI (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664. https://doi.org/10.1007/s00203-007-0286-x
Tuna LA, Kaya C, Ashraf M, Altunlu H, Yokas I, Yagmur B (2007) The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environ Exp Bot 59:173–178. https://doi.org/10.1016/j.envexpbot.2005.12.007
Tyagi NK (1986) Optimal water management strategies for salinity control. J Irrig Drain Eng 112:81–97. https://doi.org/10.1061/(ASCE)0733-9437(1986)112:2(81)
Wang J, Li X, Zhang J, Yao T, Wei D, Wang Y, Wang J (2012) Effect of root exudates on beneficial microorganisms-evidence from a continuous soybean monoculture. Plant Ecol 213:1883–1892. https://doi.org/10.1007/s11258-012-0088-3
Wang Y, Gu W, Xie T, Li L, Sun Y, Zhang H, Li J, Wei S (2016) Mixed compound of DCPTA and CCC increases maize yield by improving plant morphology and up-regulating photosynthetic capacity and antioxidants. Plos ONE 11:e0149404. https://doi.org/10.1371/journal.pone.0149404
Waqas M, Yaning C, Iqbal H, Shareef M, Rehman H, Yang Y (2017) Paclobutrazol improves salt tolerance in quinoa: beyond the stomatal and biochemical interventions. J Agron Crop Sci 203:315–322. https://doi.org/10.1111/jac.12217
Yan G, Xing Y, Xu L, Wang J, Dong X, Shan W, Guo L, Wang Q (2017) Effects of different nitrogen additions on soil microbial communities in different seasons in a boreal forest. Ecosphere 8:e01879. https://doi.org/10.1002/ecs2.1879
Yi Y, Liu Y, Luan P, Hou Z, Yang Y, Li R, Liang Z, Zhang X, Liu S (2022) Compound fermentation supernatants of antagonistic bacteria control Rhizoctonia cerealis and promote wheat growth. Egypt J Biol Pest Control 32:121. https://doi.org/10.1186/s41938-022-00620-9
Zaidi NW, Dar MH, Singh S, Singh US (2014) Trichoderma species as abiotic stress relievers in plants. In: Gupta VK, Schmoll M, Herrera-Estrella A, Upadhyay RS, Druzhinina I, Tuohy MG (eds) Biotechnology and biology of Trichoderma. Elsevier, Netherlands, pp 515–525. https://doi.org/10.1016/B978-0-444-59576-8.00038-2
Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P (2021) Regulation of plant responses to salt stress. Int J Mol Sci 22:4609. https://doi.org/10.3390/ijms22094609
Zhou XR, Dai L, Xu GF, Wang HS (2021a) A strain of Phoma species improves drought tolerance of Pinus tabulaeformis. Sci Rep 11:1–11. https://doi.org/10.1038/s41598-021-87105-1
Zhou XR, Zhang NN, Zhao YM, Dai L, Xu DP, Xu GF, Tian J (2021b) Distribution dynamics and roles of starch in non-photosynthetic vegetative organs of Santalum album Linn., a hemiparasitic tree. Front. Plant Sci 11:532537. https://doi.org/10.3389/fpls.2020.532537
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71. https://doi.org/10.1016/S1360-1385(00)01838-0
Zhu X, Cao Q, Sun L, Yang X, Yang W, Zhang H (2018) Stomatal conductance and morphology of arbuscular mycorrhizal wheat plants response to elevated CO2 and NaCl stress. Front Plant Sci 9:1363. https://doi.org/10.3389/fpls.2018.01363
Acknowledgements
We would like to thank Changliang Tang for his hospitability and the sample collection.
Funding
This research is supported by Key Scientific and Technological Projects in Henan Province (232102320093) and Special Financial Projects of Guangzhou (City–SYKH 2016165).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by XZ, XH, HW, and GX. The first draft of the manuscript was written by XH and HW. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics Approval
Not applicable
Consent to Participate
Not applicable
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Zhou, X., Huang, X., Wang, H. et al. A Strain of Cylindrocarpon spp. Promotes Salt Tolerance in Acer buergerianum. J Soil Sci Plant Nutr 24, 1134–1148 (2024). https://doi.org/10.1007/s42729-024-01616-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-024-01616-0