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Arbuscular mycorrhiza induced putrescine degradation into γ-aminobutyric acid, malic acid accumulation, and improvement of nitrogen assimilation in roots of water-stressed maize plants

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Abstract

Water shortage limits plant growth and development by inducing physiological and metabolic disorders, while arbuscular mycorrhizal (AM) symbiosis can improve plant adaptation to drought stress by altering some metabolic and signaling pathways. In this study, root growth and levels of some metabolites (polyamines, amino acids, and malic acid [MA]) and key enzymes were examined in AM-inoculated and non-inoculated (NM) maize seedlings under different water conditions. The results showed that AM symbiosis stimulated root growth and the accumulation of putrescine (Put) during initial plant growth. Root Put concentration significantly decreased in AM compared with NM plants under water stress; correspondingly, Put degradation via diamine oxidase into γ-aminobutyric acid (GABA) occurred. Moreover, glutamine concentration and the activity of N assimilation enzymes (nitrate reductase and glutamine synthetase) were higher in roots of AM than NM plants under moderate water stress. The activity of GABA transaminase and malic enzyme, and MA concentration were also higher in roots of AM than NM plants under moderate water stress. Our results indicated that Put catabolism along with improved N assimilation and the accumulation of GABA and MA were the key metabolic processes in roots of AM maize plants in response to water stress.

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References

  • Agudelo-Romero P, Bortolloti C, Pais MS, Tiburcio AF, Fortes AM (2013) Study of polyamines during grape ripening indicate an important role of polyamine catabolism. Plant Physiol Biochem 67:105–119

    CAS  PubMed  Google Scholar 

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    PubMed  Google Scholar 

  • Altamura MM, Torrigiani P, Capitani F, Scaramagli S, Bagni N (1991) De novo root formation in tobacco thin layers affected by inhibition of polyamine biosynthesis. J Exp Bot 42:1575–1582

    CAS  Google Scholar 

  • Altman A, Levin N (2006) Interactions of polyamines and nitrogen nutrition in plants. Physiol Plantarum 89(3):653–658

    Google Scholar 

  • Awasthi V, Gautam IK, Sengar RS, Garg SK (2013) Influence of putrescine on enzymes of ammonium assimilation in maize seedling. Am J Plant Sci 4:297–301

    CAS  Google Scholar 

  • Bachrach U, Wang YC, Tabib A (2001) Polyamines: new cues in cellular signal transduction. News Physiol Sci 15:106–109

    Google Scholar 

  • Bhatnagar P, Minocha R, Minocha SC (2002) Genetic manipulation of the metabolism of polyamines in poplar cells: the regulation of putrescine catabolism. Plant Physiol 128:1455–1469

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bouchereau A, Aziz AF, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    CAS  Google Scholar 

  • Bown AW, Shelp BJ (2016) Plant GABA: not just a metabolite. Trends Plant Sci 21(10):811–813

    CAS  PubMed  Google Scholar 

  • Breuninger M, Trujillo CG, Serrano E, Fischer R, Requena N (2004) Different nitrogen sources modulate activity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genet Biol 41:542–552

    CAS  PubMed  Google Scholar 

  • Brini F, Amara I, Feki K, Hanin M, Khoudi H, Masmmoudi K (2009) Physiological and molecular analyses of seedlings of two Tunisian durum wheat (Triticum turgidum L. subsp. Durum [Desf.]) varieties showing contrasting tolerance to salt stress. Acta Physiol Plant 31(1):145–154

    CAS  Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. PNAS 101(26):9909–9914

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    CAS  PubMed  Google Scholar 

  • Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945. https://doi.org/10.3389/fpls.2018.01945

    Article  PubMed  PubMed Central  Google Scholar 

  • Couée I, Hummel I, Sulmon C, Gouesbet G, Amrani AE (2004) Involvement of polyamines in root development. Plant Cell Tiss Organ 76:1–10

    Google Scholar 

  • Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loução MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144(2):782–792

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delis C, Dimou M, Flemetakis E, Aivalakis G, Katinakis P (2006) A root- and hypocotyl-specific gene coding for copper-containing amine oxidase is related to cell expansion in soybean seedlings. J Exp Bot 57(1):101–111

    CAS  PubMed  Google Scholar 

  • Du SY, Zhang XF, Lu ZK, Xin Q, Wu Z, Jiang T, Lu Y, Wang XF, Zhang DP (2012) Roles of the different components of magnesium chelatase in abscisic acid signal transduction. Plant Mol Biol 80(4–5):519–537

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13(1):14–19

    CAS  PubMed  Google Scholar 

  • Garg N, Sharma A (2019) Role of putrescine (Put) in imparting salt tolerance through modulation of put metabolism, mycorrhizal and rhizobial symbioses in Cajanus cajan (L.) Millsp. Symbiosis. https://doi.org/10.1007/s13199-019-00621-7

  • Gilliham M, Tyerman SD (2016) Linking metabolism to membrane signaling: the GABA–malate connection. Trends Plant Sci 21(4):295–301

    CAS  PubMed  Google Scholar 

  • Goicoechea N, Szalai G, Antolin MC, Sanchez-Diazl M, Paldi E (1998) Influence of arbuscular mycorrhizae and Rhizobium on free polyamines and proline levels in water-stressed alfalfa. J Plant Physiol 153:706–711

    CAS  Google Scholar 

  • Gong XQ, Zhang JY, Hu JB, Wang W, Wu H, Zhang QH, Liu JH (2015) FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant Cell Environ 38(11):2248–2262

    CAS  PubMed  Google Scholar 

  • Hu YB, Fernández V, Ma L (2014) Nitrate transporters in leaves and their potential roles in foliar uptake of nitrogen dioxide. Front Plant Sci 5:360. https://doi.org/10.3389/fpls.2014.00360

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu YB, Peuke AD, Zhao XY, Yan JX, Li CM (2019) Effects of simulated atmospheric nitrogen deposition on foliar chemistry and physiology of hybrid poplar seedlings. Plant Physiol Biochem 143(10):94–108

    CAS  PubMed  Google Scholar 

  • Huang YM, Zou YN, Wu QS (2017) Alleviation of drought stress by mycorrhizas is related to increased root H2O2 efflux in trifoliate orange. Sci Rep 7:42335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang LL, Li MJ, Zhou K, Sun TT, Hu LY, Li CY, Ma FW (2018) Uptake and metabolism of ammonium and nitrate in response to drought stress in Malus prunifolia. Plant Physiol Bioch 127:185–193

    CAS  Google Scholar 

  • Kormanik PP, Bryon WC, Schultz RC (1980) Procedures and equipment for staining large numbers of plant root samples for endomycorrhizal assay. Can J Microbiol 26(4):536–538

    CAS  PubMed  Google Scholar 

  • Kumar S, Punekar NS (1997) The metabolism of 4-aminobutyrate (GABA) in fungi. Mycol Res 101(4):403–409

    CAS  Google Scholar 

  • Kumar A, Altabella T, Taylor MA, Tiburcio AF (1997) Recent advances in polyamine research. Trends Plant Sci 2(4):124–130

    Google Scholar 

  • Legocka J, Sobieszczuk-Nowicka E, Ludwicki D, Lehmann T (2017) Putrescine catabolism via DAO contributes to proline and GABA accumulation in roots of lupine seedlings growing under salt stress. Acta Soc Bot Pol 86(3):1–11

    Google Scholar 

  • Li Z, Zhou H, Peng Y, Zhang XQ, Ma X, Huang LK, Yan YH (2015) Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regul 76:71–82

    CAS  Google Scholar 

  • Liu K, Fu H, Bei Q, Al E (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126

    CAS  Google Scholar 

  • Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827

    PubMed  PubMed Central  Google Scholar 

  • Luo Y (2009) Effects of AMF on cell membrane, endogenous polyamines, and salicylic acid in Citrus under drought stress. Huazhong Agriculture University, Master Dissertation, pp. 42 (in Chinese)

  • Mekonnen DW, Flügge UI, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci 245:25–34

    CAS  PubMed  Google Scholar 

  • Meng S, Zhang CX, Su L, Li YM, Zhao Z (2016) Nitrogen uptake and metabolism of Populus simonii in response to PEG-induced drought stress. Environ Exp Bot 123:78–87

    CAS  Google Scholar 

  • Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015

    CAS  PubMed  Google Scholar 

  • Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23

    PubMed  Google Scholar 

  • Paschalidis KA, Toumi I, Moschou PN, Roubelakis-Angelakis KA (2010) ABA-dependent amine oxidases-derived H2O2 affects stomata conductance. Plant Signal Behav 5:1153–1156

    Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62(3):869–882

    CAS  PubMed  Google Scholar 

  • Ramesh SA, Tyerman SD, Gilliham M, Xu B (2017) γ-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74:1577–1603

    CAS  PubMed  Google Scholar 

  • Ren J (2010) CuAO and its catalysate product H2O2 were involved in adventitious root formation of mung bean hypocotyl cuttings. Master Dissertation, Shaanxi Normal University (in Chinese)

  • Salazar C, Armenta JM, Cortés DF, Shulaev V (2012) Combination of an AccQ·Tag-Ultra performance liquid chromatographic method with tandem mass spectrometry for the analysis of amino acids. In: Alterman MA, Hunziker P (eds) Amino Acid Analysis: Methods and Protocols, vol 828. Methods in Molecular Biology, pp 13–28

  • Salloum MS, Menduni MF, Benavides MP, Larrauri M, Luna CM, Silvente S (2018) Polyamines and flavonoids: key compounds in mycorrhizal colonization of improved and unimproved soybean genotypes. Symbiosis 76(3):265–275

    CAS  Google Scholar 

  • Schwartz M, Altman A, Cohen Y, Arzee T (2006) Localization of ornithine decarboxylase and changes in polyamine content in root meristems of Zea mays. Physiol Plantarum 67(3):485–492

    Google Scholar 

  • Sequera-Mutiozabal M, Antoniou C, Tiburcio AF, Alcázar R, Fotopoulos V (2017) Polyamines: emerging hubs promoting drought and salt stress tolerance in plants. Curr Mol Bio Rep 3:28–36

    Google Scholar 

  • Shankar N, Khan SR, Srivastava HS (2001) The response of nitrate reductase activity and nitrate assimilation in maize roots to growth regulators at acidic pH. Biol Plant 44(4):599–601

    CAS  Google Scholar 

  • Shelp BJ, Bozzo GG, Zarei A, Simpson JP, Trobacher CP, Allan WL (2012) Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. II Integrated analysis. Botany 90(9):781–793

    CAS  Google Scholar 

  • Shen HJ, Galston AW (1985) Correlations between polyamine ratios and growth patterns in seedling roots. Plant Growth Regul 3:353–363

    CAS  PubMed  Google Scholar 

  • Song JJ, Nada K, Tachibana S (2001) The early increase of S-adenosylmethionine decarboxylase activity is essential for the normal germination and tube growth in tomato (Lycopersicon esculentum mill.) pollen. Plant Sci 161(3):507–515

    CAS  Google Scholar 

  • Su GX, Yu BJ, Zhang WH, Liu YL (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Bioch 45(8):560–566

    Google Scholar 

  • Subramanian KS, Charest C (1998) Arbuscular mycorrhizae and nitrogen assimilation in maize after drought and recovery. Physiol Plant 102:285–296

    CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221

    Google Scholar 

  • Wang W, Paschalidis K, Feng JC, Song J, Liu JH (2019) Polyamine catabolism in plants: a universal process with diverse functions. Front Plant Sci 10:561. https://doi.org/10.3389/fpls.2019.00561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu QS, Zou YN, He XH (2010) Exogenous putrescine, not spermine or spermidine, enhances root mycorrhizal development and plant growth of trifoliate orange (Poncirus trifoliata) seedlings. Int J Agric Biol 12:576–580

    Google Scholar 

  • Wu QS, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012) Arbuscular mycorrhizas alter root system architecture of citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regul 68(1):27–35

    CAS  Google Scholar 

  • Xiong YC, Li FM, Xu BC, Hodgkinson KC (2006) Hydraulic and non-hydraulic root-sourced signals in old and modern spring wheat cultivars in a semiarid area. J Plant Growth Regul 25:120–136

    CAS  Google Scholar 

  • Yang R, Yin Y, Gu Z (2015) Polyamine degradation pathway regulating growth and GABA accumulation in germinating fava bean under hypoxia-NaCl stress. J Agr Sci Tech 17:311–320

    Google Scholar 

  • Zhang F, Zou YN, Wu QS, Kuč K (2020) Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. Environ Exp Bot 171:103926. https://doi.org/10.1016/j.envexpbot.2019.103926

    Article  CAS  Google Scholar 

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Funding

The study was financially supported by the Open Fund of Key Laboratory of Dryland Agriculture, Ministry of Agriculture, P. R. China (2018KLDA02), National Key Research and Development Program of China (2016YFC0500702), and the National Natural Science Foundation of China (31800546).

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Authors and Affiliations

  1. Key Laboratory of Saline-alkali Vegetation Ecology Restoration, Ministry of Education; College of Life Science, Northeast Forestry University, 26# Hexing Road, Harbin, 150040, People’s Republic of China

    Yanbo Hu

  2. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Yanbo Hu & Baodong Chen

  3. Key Laboratory of Dryland Agriculture, Ministry of Agriculture, Bejing, People’s Republic of China

    Yanbo Hu

  4. University of Chinese Academy of Sciences, Beijing, 100049, China

    Baodong Chen

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  1. Yanbo Hu
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Hu, Y., Chen, B. Arbuscular mycorrhiza induced putrescine degradation into γ-aminobutyric acid, malic acid accumulation, and improvement of nitrogen assimilation in roots of water-stressed maize plants. Mycorrhiza 30, 329–339 (2020). https://doi.org/10.1007/s00572-020-00952-0

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