While endophytic fungi offer promising avenues for bolstering plant resilience against abiotic stressors, the molecular mechanisms behind this biofortification remain largely unknown. This study employed a multifaceted approach, combining plant physiology, proteomic, metabolomic, and targeted hormonal analyses to illuminate the early response of Brassica napus to Acremonium alternatum during the nascent stages of their interaction. Notably, under optimal growth conditions, the initial reaction to fungus was relatively subtle, with no visible alterations in plant phenotype and only minor impacts on the proteome and metabolome. Interestingly, the identified proteins associated with the Acremonium response included TUDOR 1, Annexin D4, and a plastidic K+ efflux antiporter, hinting at potential processes that could counter abiotic stressors, particularly salt stress. Subsequent experiments validated this hypothesis, showcasing significantly enhanced growth in Acremonium-inoculated plants under salt stress. Molecular analyses revealed a profound impact on the plant's proteome, with over 50% of salt stress response proteins remaining unaffected in inoculated plants. Acremonium modulated ribosomal proteins, increased abundance of photosynthetic proteins, enhanced ROS metabolism, accumulation of V-ATPase, altered abundances of various metabolic enzymes, and possibly promoted abscisic acid signaling. Subsequent analyses validated the accumulation of this hormone and its enhanced signaling. Collectively, these findings indicate that Acremonium promotes salt tolerance by orchestrating abscisic acid signaling, priming the plant's antioxidant system, as evidenced by the accumulation of ROS-scavenging metabolites and alterations in ROS metabolism, leading to lowered ROS levels and enhanced photosynthesis. Additionally, it modulates ion sequestration through V-ATPase accumulation, potentially contributing to the observed decrease in chloride content.

Department of Molecular Biology and Radiobiology Faculty of AgriSciences Mendel University in Brno Brno Czech Republic

Department of Phytology Technical University in Zvolen Zvolen Slovak Republic

Faculty of Biology Technische Universität Dresden Dresden Germany

Institute for Plant Sciences and Cluster of Excellence on Plant Sciences University of Cologne Cologne Germany

Zobrazit více v PubMed

Abdelaziz, M.E., Kim, D., Ali, S., Fedoroff, N. V. & Al‐Babili, S. (2017) The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na + /K + homeostasis under salt stress conditions. Plant Science, 263, 107–115. Available from: https://doi.org/10.1016/j.plantsci.2017.07.006.

Afzal, I., Shinwari, Z.K., Sikandar, S. & Shahzad, S. (2019) Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiological Research, 221, 36–49. Available from: https://doi.org/10.1016/j.micres.2019.02.001.

Aghajanzadeh, T.A., Reich, M., Kopriva, S. & De Kok, L.J. (2018) Impact of chloride (NaCl, KCl) and sulphate (Na2SO4, K2SO4) salinity on glucosinolate metabolism in Brassica rapa. Journal of Agronomy and Crop Science, 204, 137–146. Available from: https://doi.org/10.1111/jac.12243.

Anand, U., Pal, T., Yadav, N., Singh, V.K., Tripathi, V., Choudhary, K.K. et al. (2023) Current Scenario and Future Prospects of Endophytic Microbes: Promising Candidates for Abiotic and Biotic Stress Management for Agricultural and Environmental Sustainability. Microbial Ecology, 86, 1455–1486. Available from: https://doi.org/10.1007/s00248-023-02190-1.

Annadurai, B., Thangappan, S., Kennedy, Z.J., Patil, S.G. & Uthandi, S. (2021) Co‐inoculant response of plant growth promoting non‐rhizobial endophytic yeast Candida tropicalis VYW1 and Rhizobium sp. VRE1 for enhanced plant nutrition, nodulation, growth and soil nutrient status in Mungbean (Vigna mungo L.,). Symbiosis, 83, 115–128. Available from: https://doi.org/10.1007/s13199-020-00740-6.

Athar, H.R., Zulfiqar, F., Moosa, A., Ashraf, M., Zafar, Z.U., Zhang, L. et al. (2022) Salt stress proteins in plants: An overview. Frontiers in Plant Science, 13, 999058. Available from: https://doi.org/10.3389/fpls.2022.999058.

Auer, S. & Ludwig‐Müller, J. (2023) Biocontrol of clubroot disease: how successful are endophytic fungi and bacteria? European Journal of Plant Pathology, 167, 433–451. Available from: https://doi.org/10.1007/s10658-023-02701-3.

Azad, K. & Kaminskyj, S. (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis, 68, 73–78. Available from: https://doi.org/10.1007/s13199-015-0370-y.

Banaei‐Asl, F., Bandehagh, A., Uliaei, E.D., Farajzadeh, D., Sakata, K., Mustafa, G. & Komatsu, S. (2015) Proteomic analysis of canola root inoculated with bacteria under salt stress. Journal of Proteomics, 124, 88–111. Available from: https://doi.org/10.1016/j.jprot.2015.04.009.

Barkla, B.J., Vera‐Estrella, R., Maldonado‐Gama, M. & Pantoja, O. (1999) Abscisic Acid Induction of Vacuolar H+‐ATPase Activity in Mesembryanthemum crystallinum Is Developmentally Regulated1. Plant Physiology, 120, 811–820. Available from: https://doi.org/10.1104/pp.120.3.811.

Barth, C., Gouzd, Z.A., Steele, H.P. & Imperio, R.M. (2010) A mutation in GDP‐mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. Journal of Experimental Botany, 61, 379–394. Available from: https://doi.org/10.1093/jxb/erp310.

Berka, M., Luklová, M., Dufková, H., Berková, V., Novák, J., Saiz‐Fernández, I. et al. (2020) Barley Root Proteome and Metabolome in Response to Cytokinin and Abiotic Stimuli. Frontiers in Plant Science, 11, 590337. Available from: https://doi.org/10.3389/fpls.2020.590337.

Berková, V., Kameniarová, M., Ondrisková, V., Berka, M., Menšíková, S., Kopecká, R. et al. (2020) Arabidopsis Response to Inhibitor of Cytokinin Degradation INCYDE: Modulations of Cytokinin Signaling and Plant Proteome. Plants, 9, 1563. Available from: https://doi.org/10.3390/plants9111563.

Berková, V., Berka, M., Griga, M., Kopecká, R., Prokopová, M., Luklová, M. et al. (2022) Molecular Mechanisms Underlying Flax (Linum usitatissimum L.) Tolerance to Cadmium: A Case Study of Proteome and Metabolome of Four Different Flax Genotypes. Plants, 11, 2931. Available from: https://doi.org/10.3390/plants11212931.

Berková, V., Berka, M., Kameniarová, M., Kopecká, R., Kuzmenko, M., Shejbalová, Š. et al. (2023) Salicylic Acid Treatment and Its Effect on Seed Yield and Seed Molecular Composition of Pisum sativum under Abiotic Stress. International Journal of Molecular Sciences, 24, 5454. Available from: https://doi.org/10.3390/ijms24065454.

Cao, J., Li, X., Lv, Y. & Ding, L. (2015) Comparative analysis of the phytocyanin gene family in 10 plant species: a focus on Zea mays. Frontiers in Plant Science, 6, 515. Available from: https://doi.org/10.3389/fpls.2015.00515.

Chauhan, P., Singh, M., Sharma, A., Singh, M., Chadha, P. & Kaur, A. (2024) Halotolerant and plant growth‐promoting endophytic fungus Aspergillus terreus CR7 alleviates salt stress and exhibits genoprotective effect in Vigna radiata. Frontiers in Microbiology, 15, 1336533. Available from: https://doi.org/10.3389/fmicb.2024.1336533.

Chen, S., Wu, F., Li, Y., Qian, Y., Pan, X., Li, F. et al. (2019) NtMYB4 and NtCHS1 Are Critical Factors in the Regulation of Flavonoid Biosynthesis and Are Involved in Salinity Responsiveness. Frontiers in Plant Science, 10, 178. Available from: https://doi.org/10.3389/fpls.2019.00178.

Derbali, W., Manaa, A., Goussi, R., Derbali, I., Abdelly, C. & Koyro, H.‐W. (2021) Post‐stress restorative response of two quinoa genotypes differing in their salt resistance after salinity release. Plant Physiology and Biochemistry, 164, 222–236. Available from: https://doi.org/10.1016/j.plaphy.2021.04.024.

Dietzen, C., Koprivova, A., Whitcomb, S.J., Langen, G., Jobe, T.O., Hoefgen, R. & Kopriva, S. (2020). The Transcription Factor EIL1 Participates in the Regulation of Sulfur‐Deficiency Response. Plant Physiology, 184, 2120–2136. Available from: https://doi.org/10.1104/pp.20.01192.

Dorfer, V., Pichler, P., Stranzl, T., Stadlmann, J., Taus, T., Winkler, S. & Mechtler, K. (2014) MS Amanda, a Universal Identification Algorithm Optimized for High Accuracy Tandem Mass Spectra. Journal of Proteome Research, 13, 3679–3684. Available from: https://doi.org/10.1021/pr500202e.

Duan, L., Wang, F., Shen, H., Xie, S., Chen, X., Xie, Q. et al. (2023) Identification, evolution, and expression of GDSL‐type Esterase/Lipase (GELP) gene family in three cotton species: a bioinformatic analysis. BMC Genomics, 24, 795. Available from: https://doi.org/10.1186/s12864-023-09717-3.

Dufková, H., Berka, M., Luklová, M., Rashotte, A.M., Brzobohatý, B. & Černý, M. (2019) Eggplant Germination is Promoted by Hydrogen Peroxide and Temperature in an Independent but Overlapping Manner. Molecules, 24, 4270. Available from: https://doi.org/10.3390/molecules24234270.

Dufková, H., Berka, M., Psota, V., Brzobohatý, B. & Černý, M. (2023) Environmental impacts on barley grain composition and longevity. Journal of Experimental Botany, 74, 1609–1628. Available from: https://doi.org/10.1093/jxb/erac498.

FAOSTAT. (2022). Available from: http://www.fao.org/faostat/.

Fita, A., Rodríguez‐Burruezo, A., Boscaiu, M., Prohens, J. & Vicente, O. (2015) Breeding and Domesticating Crops Adapted to Drought and Salinity: A New Paradigm for Increasing Food Production. Frontiers in Plant Science, 6, 978. Available from: https://doi.org/10.3389/fpls.2015.00978.

Flowers, T.J., Munns, R. & Colmer, T.D. (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of Botany, 115, 419–431. Available from: https://doi.org/10.1093/aob/mcu217.

Gopalakrishnan, S., Sathya, A., Vijayabharathi, R., Varshney, R.K., Gowda, C.L.L. & Krishnamurthy, L. (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech, 5, 355–377. Available from: https://doi.org/10.1007/s13205-014-0241-x.

Han, S., Tang, R., Anderson, L.K., Woerner, T.E. & Pei, Z.‐M. 2003. A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature, 425, 196–200. Available from: https://doi.org/10.1038/nature01932.

Hao, S., Wang, Y., Yan, Y., Liu, Y., Wang, J. & Chen, S. (2021) A Review on Plant Responses to Salt Stress and Their Mechanisms of Salt Resistance. Horticulturae, 7, 132. Available from: https://doi.org/10.3390/horticulturae7060132.

Hardie, M. & Doyle, R. (2012) Measuring Soil Salinity. Plant salt tolerance: methods and protocols, 415–425. Available from: https://doi.org/10.1007/978-1-61779-986-0_28.

Harshavardhan, V.T., Van Son, L., Seiler, C., Junker, A., Weigelt‐Fischer, K., Klukas, C. et al. (2014) AtRD22 and AtUSPL1, Members of the Plant‐Specific BURP Domain Family Involved in Arabidopsis thaliana Drought Tolerance. PLoS ONE, 9, e110065. Available from: https://doi.org/10.1371/journal.pone.0110065.

Harsonowati, W., Marian, M., Surono & Narisawa, K. (2020) The Effectiveness of a Dark Septate Endophytic Fungus, Cladophialophora chaetospira SK51, to Mitigate Strawberry Fusarium Wilt Disease and With Growth Promotion Activities. Frontiers in Microbiology, 11, 585. Available from: https://doi.org/10.3389/fmicb.2020.00585

Hoch, H. C., Galvani, C. D., Szarowski, D. H., & Turner, J. N. (2005) Two new fluorescent dyes applicable for visualization of fungal cell walls. Mycologia, 97(3), 580–588. Available from: https://doi.org/10.1080/15572536.2006.11832788

Holsteens, K., De Jaegere, I., Wynants, A., Prinsen, E.L.J. & Van de Poel, B. (2022) Mild and severe salt stress responses are age‐dependently regulated by abscisic acid in tomato. Frontiers in Plant Science, 13, 982622. Available from: https://doi.org/10.3389/fpls.2022.982622.

Islam, M.M., Tani, C., Watanabe‐Sugimoto, M., Uraji, M., Jahan, MdS., Masuda, C. et al. (2009) Myrosinases, TGG1 and TGG2, Redundantly Function in ABA and MeJA Signaling in Arabidopsis Guard Cells. Plant and Cell Physiology, 50, 1171–1175. Available from: https://doi.org/10.1093/pcp/pcp066.

Jahan, N., Zhang, Y., Lv, Y., Song, M., Zhao, C., Hu, H. et al. (2020) QTL analysis for rice salinity tolerance and fine mapping of a candidate locus qSL7 for shoot length under salt stress. Plant Growth Regulation, 90, 307–319. Available from: https://doi.org/10.1007/s10725-019-00566-3.

Jan, F.G., Bibi, N., Hamayun, M., Moon, Y.‐S., Jan, G., Shafique, M. & Ali, S. (2022) Endophytic Aspergillus oryzae reprograms Abelmoschus esculentus L. to higher growth under salt stress via regulation of physiochemical attributes and antioxidant system. Biologia, 77, 2805–2818. Available from: https://doi.org/10.1007/s11756-022-01096-6.

Jäschke, D., Dugassa‐Gobena, D., Karlovsky, P., Vidal, S., & Ludwig‐Müller, J. (2010) Suppression of clubroot (Plasmodiophora brassicae) development in Arabidopsis thaliana by the endophytic fungus Acremonium alternatum. Plant Pathology, 59(1), 100–111. Available from: https://doi.org/10.1111/j.1365-3059.2009.02199.x

Jiao, Y., Zhang, J. & Pan, C. (2022) Integrated physiological, proteomic, and metabolomic analyses of pecan cultivar ‘Pawnee’ adaptation to salt stress. Scientific Reports, 12, 1841. Available from: https://doi.org/10.1038/s41598-022-05866-9.

Kashyap, P.L., Solanki, M.K., Kushwaha, P., Kumar, S. & Srivastava, A.K. (2020) Biocontrol Potential of Salt‐Tolerant Trichoderma and Hypocrea Isolates for the Management of Tomato Root Rot Under Saline Environment. Journal of Soil Science and Plant Nutrition, 20, 160–176. Available from: https://doi.org/10.1007/s42729-019-00114-y.

Khan, A.L., Hussain, J., Al‐Harrasi, A., Al‐Rawahi, A. & Lee, I.‐J. (2015) Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Critical Reviews in Biotechnology, 35, 62–74. Available from: https://doi.org/10.3109/07388551.2013.800018.

Kruasuwan, W., Lohmaneeratana, K., Munnoch, J.T., Vongsangnak, W., Jantrasuriyarat, C., Hoskisson, P.A. &Thamchaipenet, A. (2023) Transcriptome Landscapes of Salt‐Susceptible Rice Cultivar IR29 Associated with a Plant Growth Promoting Endophytic Streptomyces. Rice, 16, 6. Available from: https://doi.org/10.1186/s12284-023-00622-7.

Lee, K., Park, J., Williams, D.S., Xiong, Y., Hwang, I. & Kang, B. (2013) Defective chloroplast development inhibits maintenance of normal levels of abscisic acid in a mutant of the Arabidopsis RH 3 DEAD‐box protein during early post‐germination growth. The Plant Journal, 73, 720–732. Available from: https://doi.org/10.1111/tpj.12055.

Lee, S., Lee, E.J., Yang, E.J., Lee, J.E., Park, A.R., Song, W.H. & Park, O.K. (2004) Proteomic Identification of Annexins, Calcium‐Dependent Membrane Binding Proteins That Mediate Osmotic Stress and Abscisic Acid Signal Transduction in Arabidopsis. The Plant Cell, 16, 1378–1391. Available from: https://doi.org/10.1105/tpc.021683.

Lichtenthaler, H. K., Buschmann, C., & Knapp, M. (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica, 43(3), 379–393. https://doi.org/10.1007/s11099-005-0062-6

Lu, Y., Pang, Z. & Xia, J. (2023) Comprehensive investigation of pathway enrichment methods for functional interpretation of LC–MS global metabolomics data. Briefings in Bioinformatics, 24, bbac553. Available from: https://doi.org/10.1093/bib/bbac553.

Marian, M., Takashima, Y., Harsonowati, W., Murota, H. & Narisawa, K. (2022) Biocontrol of Pythium root rot on lisianthus using a new dark septate endophytic fungus Hyaloscypha variabilis J1PC1. European Journal of Plant Pathology, 163, 97–112. Available from: https://doi.org/10.1007/s10658-022-02459-0.

Metsalu, T. & Vilo, J. (2015) ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Research, 43, W566–W570. Available from: https://doi.org/10.1093/nar/gkv468.

Munaweera, T.I.K., Jayawardana, N.U., Rajaratnam, R. & Dissanayake, N. (2022) Modern plant biotechnology as a strategy in addressing climate change and attaining food security. Agriculture & Food Security, 11, 26. Available from: https://doi.org/10.1186/s40066-022-00369-2.

Nachshon, U. (2018) Cropland Soil Salinization and Associated Hydrology: Trends, Processes and Examples. Water, 10, 1030. Available from: https://doi.org/10.3390/w10081030.

Naheed, R., Aslam, H., Kanwal, H., Farhat, F., Abo Gamar, M.I., Al‐Mushhin, A.A.M. et al. (2021) Growth attributes, biochemical modulations, antioxidant enzymatic metabolism and yield in Brassica napus varieties for salinity tolerance. Saudi Journal of Biological Sciences, 28, 5469–5479. Available from: https://doi.org/10.1016/j.sjbs.2021.08.021.

Nomura, H., Komori, T., Kobori, M., Nakahira, Y. & Shiina, T. (2008) Evidence for chloroplast control of external Ca 2+ −induced cytosolic Ca 2+ transients and stomatal closure. The Plant Journal, 53, 988–998. Available from: https://doi.org/10.1111/j.1365-313X.2007.03390.x.

Olmos, E. (2006) Modulation of plant morphology, root architecture, and cell structure by low vitamin C in Arabidopsis thaliana. Journal of Experimental Botany, 57, 1645–1655. Available from: https://doi.org/10.1093/jxb/erl010.

Partridge, M. & Murphy, D.J. (2009) Roles of a membrane‐bound caleosin and putative peroxygenase in biotic and abiotic stress responses in Arabidopsis. Plant Physiology and Biochemistry, 47, 796–806. Available from: https://doi.org/10.1016/j.plaphy.2009.04.005.

Perez‐Riverol, Y., Bai, J., Bandla, C., García‐Seisdedos, D., Hewapathirana, S., Kamatchinathan, S. et al. (2022) The PRIDE database resources in 2022: a hub for mass spectrometry‐based proteomics evidences. Nucleic Acids Research, 50, D543–D552. Available from: https://doi.org/10.1093/nar/gkab1038.

Pino, L.K., Searle, B.C., Bollinger, J.G., Nunn, B., MacLean, B. & MacCoss, M.J. (2020) The Skyline ecosystem: Informatics for quantitative mass spectrometry proteomics. Mass Spectrometry Reviews, 39, 229–244. Available from: https://doi.org/10.1002/mas.21540.

Polle, A. & Chen, S. (2015) On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant, Cell & Environment, 38, 1794–1816. Available from: https://doi.org/10.1111/pce.12440.

Raps, A. & Vidal, S. (1998) Indirect effects of an unspecialized endophytic fungus on specialized plant ‐ herbivorous insect interactions. Oecologia, 114, 541–547. Available from: https://doi.org/10.1007/s004420050478.

Raza, A., Tabassum, J., Fakhar, A.Z., Sharif, R., Chen, H., Zhang, C. et al. (2023) Smart reprograming of plants against salinity stress using modern biotechnological tools. Critical Reviews in Biotechnology, 43, 1035–1062. Available from: https://doi.org/10.1080/07388551.2022.2093695.

Redecker, D., Kodner, R. & Graham, L.E. (2000) Glomalean Fungi from the Ordovician. Science, 289, 1920–1921. Available from: https://doi.org/10.1126/science.289.5486.1920.

Rho, H., Hsieh, M., Kandel, S.L., Cantillo, J., Doty, S.L. & Kim, S.‐H. (2018) Do Endophytes Promote Growth of Host Plants Under Stress? A Meta‐Analysis on Plant Stress Mitigation by Endophytes. Microbial Ecology, 75, 407–418. Available from: https://doi.org/10.1007/s00248-017-1054-3.

Rodríguez‐Milla, M.A. & Salinas, J. (2009) Prefoldins 3 and 5 Play an Essential Role in Arabidopsis Tolerance to Salt Stress. Molecular Plant, 2, 526–534. Available from: https://doi.org/10.1093/mp/ssp016.

Romero, D., Rivera, M.E., Cazorla, F.M., De Vicente, A. & Pérez‐garcía, A. (2003) Effect of mycoparasitic fungi on the development of Sphaerotheca fusca in melon leaves. Mycological Research, 107, 64–71. Available from: https://doi.org/10.1017/S0953756202006974.

Salem, M.A., Yoshida, T., Perez de Souza, L., Alseekh, S., Bajdzienko, K., Fernie, A.R. & Giavalisco, P. (2020) An improved extraction method enables the comprehensive analysis of lipids, proteins, metabolites and phytohormones from a single sample of leaf tissue under water‐deficit stress. The Plant Journal, 103, 1614–1632. Available from: https://doi.org/10.1111/tpj.14800.

Sarkar, B., Bandyopadhyay, P., Das, A., Pal, S., Hasanuzzaman, M. & Adak, M.K. (2023) Abscisic acid priming confers salt tolerance in maize seedlings by modulating osmotic adjustment, bond energies, ROS homeostasis, and organic acid metabolism. Plant Physiology and Biochemistry, 202, 107980. Available from: https://doi.org/10.1016/j.plaphy.2023.107980.

Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675. Available from: https://doi.org/10.1038/nmeth.2089.

Seppelt, R., Klotz, S., Peiter, E. & Volk, M. (2022) Agriculture and food security under a changing climate: An underestimated challenge. iScience, 25, 105551. Available from: https://doi.org/10.1016/j.isci.2022.105551.

Shahid, S.A., Zaman, M. & Heng, L. (2018) Soil Salinity: Historical Perspectives and a World Overview of the Problem. In: Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques. Cham: Springer International Publishing, 43–53. Available from: https://doi.org/10.1007/978-3-319-96190-3_2.

Shahzad, B., Rehman, A., Tanveer, M., Wang, L., Park, S.K. & Ali, A. (2022) Salt Stress in Brassica: Effects, Tolerance Mechanisms, and Management. Journal of Plant Growth Regulation, 41, 781–795. Available from: https://doi.org/10.1007/s00344-021-10338-x.

Śliżewska, W., Struszczyk‐Świta, K. & Marchut‐Mikołajczyk, O. (2022) Metabolic Potential of Halophilic Filamentous Fungi—Current Perspective. International Journal of Molecular Sciences, 23, 4189. Available from: https://doi.org/10.3390/ijms23084189.

Su, H.‐G., Zhang, X.‐H., Wang, T.‐T., Wei, W.‐L., Wang, Y.‐X., Chen, J. et al. (2020) Genome‐Wide Identification, Evolution, and Expression of GDSL‐Type Esterase/Lipase Gene Family in Soybean. Frontiers in Plant Science, 11, 726. Available from: https://doi.org/10.3389/fpls.2020.00726.

Su, W., Raza, A., Gao, A., Jia, Z., Zhang, Y., Hussain, M.A. et al. (2021) Genome‐Wide Analysis and Expression Profile of Superoxide Dismutase (SOD) Gene Family in Rapeseed (Brassica napus L.) under Different Hormones and Abiotic Stress Conditions. Antioxidants, 10, 1182. Available from: https://doi.org/10.3390/antiox10081182.

Summerbell, R.C., Gueidan, C., Schroers, H.‐J., de Hoog, G.S., Starink, M., Rosete, Y.A. et al. (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Studies in Mycology, 68, 139–162. Available from: https://doi.org/10.3114/sim.2011.68.06.

Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta‐Cepas, J. et al. (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome‐wide experimental datasets. Nucleic Acids Research, 47, D607–D613. Available from: https://doi.org/10.1093/nar/gky1131.

Verma, A., Shameem, N., Jatav, H.S., Sathyanarayana, E., Parray, J.A., Poczai, P. & Sayyed, R.Z. (2022) Fungal Endophytes to Combat Biotic and Abiotic Stresses for Climate‐Smart and Sustainable Agriculture. Frontiers in Plant Science, 13, 953836. Available from: https://doi.org/10.3389/fpls.2022.953836.

Wang, Y., Stevanato, P., Lv, C., Li, R. & Geng, G. (2019) Comparative Physiological and Proteomic Analysis of Two Sugar Beet Genotypes with Contrasting Salt Tolerance. Journal of Agricultural and Food Chemistry, 67, 6056–6073. Available from: https://doi.org/10.1021/acs.jafc.9b00244.

Xiong, L., Lee, B., Ishitani, M., Lee, H., Zhang, C. & Zhu, J.‐K. (2001) FIERY1 encoding an inositol polyphosphate 1‐phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes & Development, 15, 1971–1984. Available from: https://doi.org/10.1101/gad.891901.

Xu, T., Lee, K., Gu, L., Kim, J.‐I. & Kang, H. (2013) Functional characterization of a plastid‐specific ribosomal protein PSRP2 in Arabidopsis thaliana under abiotic stress conditions. Plant Physiology and Biochemistry, 73, 405–411. Available from: https://doi.org/10.1016/j.plaphy.2013.10.027.

Xue, T., Wan, H., Chen, J., He, S., Lujin, C., Xia, M. et al. (2024) Genome‐wide identification and expression analysis of the chlorophyll a/b binding protein gene family in oilseed (Brassica napus L.) under salt stress conditions. Plant Stress, 11, 100339. Available from: https://doi.org/10.1016/j.stress.2023.100339.

Yan, C., Yan, Z., Wang, Y., Yan, X. & Han, Y. (2014) Tudor‐SN, a component of stress granules, regulates growth under salt stress by modulating GA20ox3 mRNA levels in Arabidopsis. Journal of Experimental Botany, 65, 5933–5944. Available from: https://doi.org/10.1093/jxb/eru334.

Yang, X., Song, B., Cui, J., Wang, L., Wang, S., Luo, L. et al. (2021) Comparative ribosome profiling reveals distinct translational landscapes of salt‐sensitive and ‐tolerant rice. BMC Genomics, 22, 612. Available from: https://doi.org/10.1186/s12864-021-07922-6.

Yao, L., Wang, H., Wan, Z., Li, R. & Yu, J. (2019) The High Diversity and Variable Susceptibility of Clinically Relevant Acremonium‐Like Species in China. Mycopathologia, 184, 759–773. Available from: https://doi.org/10.1007/s11046-019-00399-8.

Yonamine, I., Yoshida, K., Kido, K., Nakagawa, A., Nakayama, H. & Shinmyo, A. (2004) Overexpression of NtHAL3 genes confers increased levels of proline biosynthesis and the enhancement of salt tolerance in cultured tobacco cells. Journal of Experimental Botany, 55, 387–395. Available from: https://doi.org/10.1093/jxb/erh043.

Yuan, Y., Li, J., Zhang, M., Yang, Q., & Feng, B. (2023) Broomcorn millet (Panicum miliaceum L.) tolerates soil salinity by regulating salt‐tolerance mechanism and reshaping rhizosphere microorganisms. Plant and Soil, 492, 261–284. Available from: https://doi.org/10.1007/s11104-023-06170-9

Zhang, H., Song, J., Dong, F., Li, Y., Ge, S., Wei, B. & Liu, Y. (2023) Multiple roles of wheat ferritin genes during stress treatment and TaFER5D‐1 as a positive regulator in response to drought and salt tolerance. Plant Physiology and Biochemistry, 202, 107921. Available from: https://doi.org/10.1016/j.plaphy.2023.107921.

Zhang, S., Gan, Y. & Xu, B. (2019) Mechanisms of the IAA and ACC‐deaminase producing strain of Trichoderma longibrachiatum T6 in enhancing wheat seedling tolerance to NaCl stress. BMC Plant Biology, 19, 22. Available from: https://doi.org/10.1186/s12870-018-1618-5.

Zheng, S., Su, M., Shi, Z., Gao, H., Ma, C., Zhu, S. et al. (2022) Exogenous sucrose influences KEA1 and KEA2 to regulate abscisic acid‐mediated primary root growth in Arabidopsis. Plant Science, 317, 111209. Available from: https://doi.org/10.1016/j.plantsci.2022.111209.

Zhu, J.‐K. (2001) Plant salt tolerance. Trends in Plant Science, 6, 66–71. Available from: https://doi.org/10.1016/S1360-1385(00)01838-0.

Antioxidant Responses and Redox Regulation Within Plant-Beneficial Microbe Interaction