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Adenosine 5′-monophosphate decreases citrate exudation and aluminium resistance in Tamba black soybean by inhibiting the interaction between 14-3-3 proteins and plasma membrane H+-ATPase

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Abstract

Our previous study suggested that aluminium (Al) stress increased plasma membrane (PM) H+-ATPase activity and citrate secretion and simultaneously enhanced the interaction between 14-3-3 proteins and phosphorylated PM H+-ATPase in Al-resistant Tamba black soybean (RB). Adenosine 5′-monophosphate (AMP) is known as an inhibitor of the interaction between 14-3-3 proteins and PM H+-ATPases. To investigate the effects of AMP on Al resistance, PM H+-ATPase activity and citrate exudation, AMP was used to treat Al-stressed RB. The results showed that after treatment with either 100 μM AMP or 50 μM Al for 8 h, RB root growth was inhibited by approximately 50 and 30%, respectively. However, simultaneous treatment with 100 μM AMP and 50 μM Al for 8 h resulted in a 60% inhibition of RB root growth, indicating that the presence of AMP reduced Al tolerance in RB. The interaction of PM H+-ATPase and 14-3-3 proteins in the root tips of Al-treated RB was stronger than that in the untreated control. However, the interaction of the two proteins was greatly reduced (lower than that in the control) after co-treatment with Al and AMP, suggesting that the presence of AMP under Al stress reduced the Al-enhanced interaction between PM H+-ATPase and 14-3-3 proteins. Consequently, PM H+-ATPase activity decreased by approximately 50%, which led to a significant decrease in H+ efflux and citrate secretion in RB roots under Al stress. Collectively, these results indicate that AMP reduced citrate exudation and Al resistance in RB by inhibiting the interaction between 14-3-3 proteins and PM H+-ATPases under Al stress.

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References

  • Athwal GS, Huber JL, Huber SC (1998) Phosphorylated nitrate reductase and 14-3-3 proteins: the site of interaction, effects of ions, and evidence for an AMP binding site on 14-3-3 proteins. Plant Physiol 118:1041–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Athwal GS, Lombardo CR, Huber JL, Masters SC, Fu H, Huber SC (2000) Modulation of 14-3-3 protein interactions with target polypeptides by physical and metabolic effectors. Plant Cell Physiol 41:523–533

    Article  CAS  PubMed  Google Scholar 

  • Bachmann M, Huber JL, Liao PC, Gage DA, Huber SC (1996) The inhibitor protein of phosphorylated nitrate reductase from spinach (Spinacia oleracea L.) leaves is a 14-3-3 protein. FEBS Lett 387:127–131

    Article  CAS  PubMed  Google Scholar 

  • Camoni L, Iori V, Marra M, Aducci P (2000) Phosphorylation-dependent interaction between plant plasma membrane H-ATPase and 14-3-3 proteins. J Biol Chem 275:9919–9923

    Article  CAS  PubMed  Google Scholar 

  • Camoni L, Visconti S, Marra M, Aducci P (2001) Adenosine 5′-Monophosphate inhibits the association of14-3-3 protein with the plant plasma membrane H+-ATPase. J Biol Chem 276:31709–31712

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Wu K-H, Zhang Y-N, Phan X-H, Li K-Z, Yu Y-X, Chen L-M (2012) Physiological and molecular responses of broad bean (Vicia faba L.) to aluminum stress. Acta Physiol Plant 34:2251–2263

    Article  CAS  Google Scholar 

  • Chen Q, Guo CL, Wang P, Chen XQ, Wu KH, Li KZ, Yu YX, Chen LM (2013) Up-regulation and interaction of the plasma membrane H+-ATPase and the 14-3-3 protein are involved in the regulation of citrate exudation from the broad bean (Vicia faba L.) under Al stress. Plant Physiol Bioch 70:504–511

    Article  CAS  Google Scholar 

  • De Azevedo Neto AD, Prisco JT, Enéas-Filho J, Rolim Medeiros JV, Gomes-Filho E (2005) Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol 162:1114–1122

    Article  PubMed  Google Scholar 

  • Glaab J, Kaiser WM (1993) Rapid modulation of nitrate reductase in pea roots. Planta 191:173–179

    Article  CAS  Google Scholar 

  • Guo CL, Chen Q, Chen XQ, Zhao Y, Zhao XL, Wang L, Li KZ, Yu YX, Chen LM (2013) Al-enhanced expression and Interaction of14-3-3 protein and plasma membrane H+-ATPase is related to al-induced citrate secretion in an al-resistant black soybean. Plant Mol Biol Rep 31:1012–1024

    Article  CAS  Google Scholar 

  • Huber SC, Kaiser WM (1996) 5-Aminoimidazole-4-carboxamide riboside activates nitrate reductase in darkened spinach and pea leaves. Physiol Plant 98:833–837

    Article  CAS  Google Scholar 

  • Huber SC, Mackintosh C, Kaiser WM (2002) Metabolic enzymes as targets for 14-3-3 proteins. Plant Mol Bio 50:1053–1063

    Article  CAS  Google Scholar 

  • Kaiser WM, Huber S (1994) Modulation of nitrate reductase in vivo and in vitro: effects of phosphoprotein phosphatase inhibitors, free Mg2 + and 5′-. AMPPlanta 193:358–364

    CAS  Google Scholar 

  • Kaiser WM, Huber SC (2001) Regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52:1981–1989

    Article  CAS  PubMed  Google Scholar 

  • Kaiser WM, Spill D (1991) Rapid modulation of spinach leaf nitrate reductase activity by photosynthesis II. In vitro-modulation by ATP and AMP. Plant Physiol 96:368–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser WM, Spill D, Brendle-Behnisch E (1992) Adenine nucleotides are apparently involved in the light-dark modulation of spinach leaf nitrate reductase. Planta 186:236–240

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Park W, Nian H, Sasaki T, Ezaki B, Jang YS, Chung GC, Bae HJ, Ahn SJ (2010) Aluminum tolerance associated with enhancement of plasma membrane H+-ATPase in the root apex of soybean. Soil Sci Plant Nutr 56:140–149

    Article  CAS  Google Scholar 

  • Ligaba A, Yamaguchi M, Shen H, Sasaki T, Yamamoto Y, Matsumoto H (2004) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Funct Plant Biol 31:1075–1083

    Article  CAS  Google Scholar 

  • Ohno T, Koyama H, Hara T (2003) Characterization of citrate transport through the plasma membrane in a carrot mutant cell line with enhanced citrate excretion. Plant Cell Physiol 44:156–162

    Article  CAS  PubMed  Google Scholar 

  • Reggiani R, Mattana M, Aurisano N, Bertani A (1993) Utilization of stored nitrate during the anaerobic germination of rice seeds. Plant Cell Physiol 34:379–383

    CAS  Google Scholar 

  • Sabina RL, Patterson D, Holmes EW (1985) 5-Amino-4-imidazolecarboxamide riboside (Z-riboside) metabolism in eukaryotic cells. J Bio Chem 260:6107–6114

    CAS  Google Scholar 

  • Sehnke PC, DeLille JM, Ferl RJ (2002) Consummating signal transduction: the role of 14-3-3 proteins in the completion of signal-induced transitions in protein activity. Plant Cell 14(Sup):339–354

    Article  Google Scholar 

  • Shen H, He L, Sasaki T, Yamamoto Y, Zheng S, Ligaba A, Yan X, Ahn S, yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress: up-regulation of transcription, translation, and threonine-oriented phosphorylation, of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan JE, Carey F, Carling D, Beri RK (1994) Characterisation of 5′-AMP-activated protein kinase in human liver using specific peptide substrates and the effects of 5′-AMP analogues on enzyme activity. Biochem Bioph Res Co 200:1551–1556

    Article  CAS  Google Scholar 

  • Tomasi N, Kretzschmar T, Espen L, weisskopf L, Fuglsang A, Palmgren M, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32:465–475

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Zhu XF, Peng YX, Zheng C, Ming F, Zheng SJ (2011) Aluminum regulates oxalate secretion and plasma membrane H+-ATPase activity independently in tomato roots. Planta 234:281–291

    Article  CAS  PubMed  Google Scholar 

  • Yang D, Chen D, Wang P (2017) Aluminium-inhibited NO3 - uptake is related to Al-increased H2O2 content and Al-decreased plasma membrane ATPase activity in the root tips of Al-sensitive black soybean. Funct Plant Biol 44:198–207

    Article  CAS  Google Scholar 

  • Zhou XH, Gu ZH, Xu HN, Chen LM, Tao GX, Yu YX, Li KZ (2016) The effects of exogenous ascorbic acid on the mechanism of physiological and biochemical responses to nitrate uptake in two rice cultivars (Oryza sativa L.) under aluminum stress. Plant Growth Regul 35:1013–1024

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported in part by the grant of the National Natural Science Foundation of China (No. 31260063), the grant of the National Basic Research Program of China (No. 2014CB138701) and by the grant of Yunnan Applied Basic Research Projects of China (No. 2013FZ120). We are grateful for the instrument assistance of Prof Kunzhi Li, Kunming University of Science and Technology for this study.

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  1. Yong Min and Chuan-Long Guo have contributed equally to this work.

Authors and Affiliations

  1. Faculty of Environmental Science and Engineering, Kunming University of Science and Technology, Chenggong, Kunming, 650500, China

    Yong Min

  2. Biotechnology Research Centre, Faculty of Life Science and Biotechnology, Kunming University of Science and Technology, Chenggong Campus, Chenggong, Kunming, 650500, China

    Yong Min, Chuan-Long Guo, Xiu-Ling Zhao, Lin Wang & Li-Mei Chen

  3. College of Zoological Science and Technology, Southwest University, Chongqing, 400715, China

    Yong-Xiong Yu

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  1. Yong Min
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  2. Chuan-Long Guo
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  4. Lin Wang
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  5. Yong-Xiong Yu
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  6. Li-Mei Chen
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Correspondence to Li-Mei Chen.

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Min, Y., Guo, CL., Zhao, XL. et al. Adenosine 5′-monophosphate decreases citrate exudation and aluminium resistance in Tamba black soybean by inhibiting the interaction between 14-3-3 proteins and plasma membrane H+-ATPase. Plant Growth Regul 84, 285–292 (2018). https://doi.org/10.1007/s10725-017-0339-3

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