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Root Exudates Response of Mycorrhizal Pinus massoniana Seedlings Under Drought Stress

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Abstract

Pinus massoniana Lamb. (P. massoniana) grown under water-deficient conditions displays a series of coordinated adaptive responses. Although ectomycorrhizal (ECM) fungi can enhance plant adaptation to water deficiency, the research of ECM fungi colonization and water stress intensity induce P. massoniana seedlings root exudates to resist is no depth. One-year-old P. massoniana seedlings without inoculation (St1) and inoculated with Suillus luteus (St2, St3) were studied under no water stress 70–80% (Wt1), mild stress 60–70% (Wt2), moderate stress 50–60% (Wt3), and severe stress 35–50% (Wt4), respectively. The root exudates of seedlings were extracted by organic extraction method and identified by gas chromatography-mass spectrometry (GC–MS). The results show that root exudates variety and contents of different seedlings decreased as drought stress increased. Except for St1 under Wt1 treatment, other seedlings root secreted mono (2-ethylhexyl) phthalate (MEHP). Under the same water treatment, MEHP content of seedlings was Wt2: St1 (17.74%) < St3 (21.04%) < St2 (23.67%), Wt3: St1 (76.46%) < St2 (77.35%) < St3 (77.82%), and Wt4: St1 (0%) < St3 (56.71%) < St2 (61.65%). The content of MEHP in mycorrhizal P. massoniana seedlings was higher than that of un-inoculated seedlings. Therefore, drought can reduce root exudates richness of P. massoniana seedlings and the more obvious difference was that ECM fungi can increase the content of MEHP in seedlings significantly. The change was likely an important feature of mycorrhiza P. massoniana seedlings to adapt to drought stress.

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Data Availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Albert GG, Catherine P, Jordi S, Michal O, Otmar U, Josep P (2018) Root exudate metabolomes change under drought and show limited capacity for recovery. Sci Rep 8:12696

    Article  Google Scholar 

  • Calvo OC, Franzaring J, Schmid I, Fangmeier A (2019) Root exudation of carbohydrates and cations from barley in response to drought and elevated CO2. Plant Soil 438(1/2):127–142

    Article  CAS  Google Scholar 

  • Canarini A, Merchant A, Dijkstra FA (2016) Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere 2:85–97

    Article  Google Scholar 

  • Chen Y, Yao Z, Sun Y, Wang E, Tian C, Sun Y, Liu J, Sun C, Tian L (2022) Current studies of the effects of drought stress on root exudates and rhizosphere microbiomes of crop plant species. Int J Mol Sci 23:2374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Vries FT, Williams A, Stringer F, Willcocks R, McEwing R, Langridge H, Straathof AL (2019) Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling. New Phytol 224:132–145

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan FH, Ding GJ, Wen XP (2016) Proteomic analyses provide new insights into the responses of Pinus massoniana seedlings to phosphorus deficiency. Proteomics 16:504–515

    Article  CAS  PubMed  Google Scholar 

  • Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Change Biol 21(5):2082–2094

    Article  ADS  Google Scholar 

  • Gargallo-Garriga A, Preece C, Sardans J, Oravec M, Urban O, Penuelas J (2018) Root exudate metabolomes change under drought and show limited capacity for recovery. Sci Rep 8(1):1–15

    Article  CAS  Google Scholar 

  • Gomez-cadenas A, Vives V, Zandalinas SI, Manzi M, Sánchez-Pérez AM, Pérez-Clemente RM, Arbona V (2015) Abscisic acid: a versatile phytohormone in plant signaling and beyond. Curr Protein Pept Sci 16(5):413–434

    Article  CAS  PubMed  Google Scholar 

  • Gu X, Ni Y, Jiang Y, Hao J (2018) Effects of laccaria bicolor on growth, uptake and distribution of nutrients and aluminum of Pinus massoniana seedlings under acid aluminum exposure. Sci Silvae Sin 54(2):170–178

    CAS  Google Scholar 

  • Henry A, Doucette W, Norton J, Bugbee B (2007) Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. J Environ Qual 36(3):904–912

    Article  CAS  PubMed  Google Scholar 

  • Jakoby G, Rog I, Megidish S, Klein T (2020) Enhanced root exudation of mature broadleaf and conifer trees in a Mediterranean forest during the dry season. Tree Physiol 40(11):1595–1605

    Article  PubMed  Google Scholar 

  • Jiang YM, Zhang SL, Lv MK, Xiong XL, Li JY, Cao AN, Xie JH (2022) Effects of Ectomycorrhizal exclusion on soil enzyme activities in Pinus massoniana plantation in red soil erosion area. J Subtrop Resour Environ 17(2):17–22 ((in Chinense))

    Google Scholar 

  • Li M, Zhao XZ, Wang HY, Lu ZK, Ding GJ (2020) Effects of drought stress and ectomycorrhizal fungi on the root morphology and exudates of Pinus massoniana seedlings. Sci Silvae Sin 58(7):63–72 ((In Chinese))

    CAS  Google Scholar 

  • Li M, Wang HY, Zhao XZ, Lu ZK, Sun XG, Ding GJ (2021a) Role of Suillus placidus in improving the drought tolerance of masson pine (Pinus massoniana Lamb.) seedlings. Forests 12(3):332

    Article  Google Scholar 

  • Li X, Kang W, Liu S, Yin H, Lyu Q, Su Y, Liu J, Liu J, Fan C, Chen G, Zhao K, Li X (2021b) Diversity of ectomycorrhizal fungal communities in four types of stands in Pinus massoniana plantation in the west of China. Forests 12:719

    Article  Google Scholar 

  • Luo XM, Ding GJ, Wang Y (2018) Active constituents of soil extracts from mycorrhizal seedling rhizosphere of Pinus massoniana and their effects on seed germination. Sci Silvae Sin 54(8):32–38 ((in Chinese))

    CAS  Google Scholar 

  • Mrak T, Straus I, Grebenc T, Gričar J, Hoshika Y, Carriero G, Paoletti E, Kraigher H (2019) Different belowground responses to elevated ozone and soilwater deficit in three Europeanoak species (Quercus ilex, Q. pubescens and Q. robur). Sci Total Environ 651(1):1310–1320

    Article  ADS  CAS  PubMed  Google Scholar 

  • Oburger E, Jones DL (2018) Sampling root exudates-mission impossible? Rhizosphere 6:116–133

    Article  Google Scholar 

  • Peng JF, Liu Y, Peng M, Wei XX, Li JK, Cui JY, Li X, Li JR (2023) Diverging growth and resilience of Pinus tabulaeformis and Pinus massoniana to droughts in north-south transition zone, central China. Dendrochronologia 78:126060

    Article  Google Scholar 

  • Pino NJ, Muñera LM, Peñuela GA (2016) Root exudates and plant secondary metabolites of different plants enhance polychlorinated biphenyl degradation by rhizobacteria. Bioremediat J 20(2):108–116

    Article  CAS  Google Scholar 

  • Pye MF, Dye SM, Resende RS, Macdonald JD, Bostock RM (2018) Abscisic acid as a dominant signal in tomato during salt stress predisposition to Phytophthora root and crown rot. Front Plant Sci 9:525

    Article  PubMed  PubMed Central  Google Scholar 

  • Quan WX, Ding GJ (2017) Root tip structure and volatile organic compound responses to drought stress in Masson pine (Pinus massoniana Lamb.). Acta Physiol Plant 39:258

    Article  Google Scholar 

  • Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, García-Mina JM, Ruyter-Spira C, López-Ráez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39:441–452

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-arcos C, Kai M, Svato A, Gershenzon J, Kunert G (2019) Untargeted metabolomics approach reveals differences in host plant chemistry before and after infestation with different pea aphid host races. Front Plant Sci 10:188

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen M, Huang W, Chen M, Song B, Zeng G, Zhang Y (2020) (Micro) plastic crisis: Un-ignorable contribution to global greenhouse gas emissions and climate change. J Clean Prod 254:120138

    Article  CAS  Google Scholar 

  • Song FB, Han XY, Zhu XC, Herbert SJ (2012) Response to water stress of soil enzymes and root exudates from drough and non-drought tolerant corn hybrids at different growth stages. Rev Can Sci Sol 92(3):501–507

    Article  CAS  Google Scholar 

  • Stermitz F, Vivanco JM (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146(2):762–771

    PubMed  PubMed Central  Google Scholar 

  • Surender Reddy P, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kavi Kishor PB (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113

    Article  CAS  PubMed  Google Scholar 

  • Suz LM, Bidartondo MI, van der Linde S, Kuyper TW (2021) Ectomycorrhizas and tipping points in forest ecosystems. New Phytol 231:1700–1707

    Article  PubMed  Google Scholar 

  • Szuba A, Marczak Ł, Kozłowski R (2021) Pb stress and ectomycorrhizas: strong protective proteomic responses in poplar roots inoculated with Paxillus involutus isolate and characterized by low root colonization intensity. Mol Sci 22(9):4300

    Article  CAS  Google Scholar 

  • Techer D, Laval-Gilly P, Henry S, Bennasroune A, Formanek P, Martinez-Chois C, D’Innocenzo M, Muanda F, Dicko A, Rejsek K, Falla J (2011) Contribution of Miscanthus x giganteus root exudates to the biostimulation of PAH degradation: an in vitro study. Sci Total Environ 409(20):4489–4495

    Article  ADS  CAS  PubMed  Google Scholar 

  • Teh CY, Mahmood M, Shaharuddin NA, Ho CL (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(3):771–781

    Article  CAS  Google Scholar 

  • Vives-peris V, Gomez-Cadenas A, Perezclemente RM (2017) Citrus plants exude proline and phytohormones under abiotic stress conditions. Plant Cell Rep 36(12):1971–1984

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Tu GY (2021) Effects of drought and rewatering on physiological properties of five species of Pinus massoniana seedlings. J Central South Univ for Technol 41(4):20–30 ((in Chinese))

    Google Scholar 

  • Wang X, Tang C, Severi J, Butterly CR, Baldock JA (2016) Rhizosphere priming effect on soil organic carbon decomposition under plant species differing in soil acidification and root exudation. New Phytol 211(3):864–873

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Tian ZM, Tunlid A, Persson P (2020) Nitrogen acquisition from mineral-associated proteins by an ectomycorrhizal fungus. New Phytol 228(2):697–711

    Article  CAS  PubMed  Google Scholar 

  • Williams A, de Vries FT (2020) Plant root exudation under drought: implications for ecosystem functioning. New Phytol 225:1899–1905

    Article  PubMed  Google Scholar 

  • Xu C, Wu XQ (2016) Physiological and proteomic analysis of mycorrhizal Pinus massoniana inoculated with lactarius insulsus under drought stress. Russ J Plant Physl 63(5):709–717

    Article  CAS  Google Scholar 

  • Yu P, Sun Y, Huang Z, Zhu F, Sun Y, Jiang L (2020) The effects of ectomycorrhizal fungi on heavy metals’ transport in Pinus massoniana and bacteria community in rhizosphere soil in mine tailing area. J Hazard Mater 381:121203

    Article  CAS  PubMed  Google Scholar 

  • Zhang N, Wang DD, Liu YP, Li SQ, Shen QR, Zhang RF (2014) Effects of different plant root exudates and their organic acid components on chemotaxis biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374(1/2):689–700

    Article  CAS  Google Scholar 

  • Zhang SZ, Li YH, Kong CH, Xu XH (2016) Interference of allelopathic wheat with different weeds. Pest Manag Sci 72(1):172–178

    Article  PubMed  Google Scholar 

  • Zhang M, Cai Z, Zhang G, Zhang D, Pan X (2021) Abiotic mechanism changing tetracycline resistance in root mucus layer of floating plant: the role of antibiotic-exudate complexation. J Hazard Mater 5(23):416

    Google Scholar 

  • Zhou Y, Tang N, Hang L, Zhao Y, Tang X, Wang K (2018) Effects of salt stress on plant growth, antioxidant capacity, glandular trichome density, and volatile exudates of Schizonepeta tenuifolia briq. Int J Mol Sci 19(1):E252

    Article  Google Scholar 

  • Zou YN, Srivastava AK, Ni QD, Wu QS (2015) Disruption of mycorrhizal extraradical mycelium and changes in leaf water status and soil aggregate stability in rootbox-grown trifoliate orange. Front Microbiol 6:203

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Professor Guijie Ding of Guizhou University and Associate Professor Yi Wang of Guizhou University for Nationalities for their support and help to the project. The strains were provided by Professor Jianguo Huang of Southwest University. The excellent forest stands in Duyun City, Guizhou Province, provided P. massoniana seeds.

Funding

This research was supported by the National Natural Science Foundation (NSFC) (32360379); Guizhou Provincial Basic Research Program of Natural Science (qjhe-ZK[2022]General207); Youth Scientific and Technological Talent Growth Project of Guizhou Provincial Department of Education (qjhe KY [2018]134); and the Natural Science Foundation of Guizhou Minzu University (gzmu [2019] yb18).

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YW designed the research, provided guidance, and reviewed the manuscript; QC analyzed data, drew the drawings, and then wrote and revised the manuscript; HH performed the experiments and collected data; WZ assisted in the experiments and manuscript. All authors read and approved the final manuscript.

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Correspondence to Yi Wang.

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Wang, Y., Chen, Q., Hu, H. et al. Root Exudates Response of Mycorrhizal Pinus massoniana Seedlings Under Drought Stress. J Plant Growth Regul 43, 576–588 (2024). https://doi.org/10.1007/s00344-023-11115-8

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