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Effects of three phenolic compounds on mitochondrial function and root vigor of cotton (Gossypium hirsutum L.) seedling roots

  • Guowei Zhang
  • Changqin Yang
  • Ruixian LiuEmail author
  • Wanchao Ni
Original Article
  • 55 Downloads

Abstract

Continuous cropping of cotton causes accumulation of allelochemicals in soil that results in substantial crop yield and quality losses. To elucidate the physiological mechanism of the effects of allelochemicals on cotton root growth, and solve the problem of continuous cropping obstacles, hydroponics experiments were carried out to study the effects of three allelochemicals (p-hydroxybenzoic acid (PHBA), phloroglucinol, and ferulic acid) at different concentrations (0.8, 4.0, and 20.0 mmol L−1) on the production of reactive oxygen species, antioxidant enzyme activities, and mitochondrial function of cotton seedling roots. All three phenolic compounds suppressed cotton root growth, decreased the activity of antioxidant enzymes (superoxide dismutase, catalase and peroxidase) and H+-ATPase in root mitochondria, and increased generation of O2 and the content of H2O2. They also increased the degree of openness of mitochondria permeability transition pores, and decreased the membrane fluidity of mitochondria, and the ratio of cytochrome (Cyt) c/a, thus resulting in the damage of mitochondrial structure and overall function of the root system. Ferulic acid at 20.0 mmol L−1 inhibited cotton root growth more than the other treatments. Above all, all three kinds of allelochemicals inhibited antioxidant enzyme activity and mitochondrial function in cotton seedling roots, and the inhibition depended on the dose of phenolic compounds. Compared to PHBA and phloroglucinol, ferulic acid was a stronger inhibitor of cotton seedling root growth.

Keywords

Cotton Phenolic compounds Mitochondrial function Root vigor Root 

Notes

Acknowledgements

This research was supported by the National Key Research and Development Program of China (2017YFD0201900), the Science and Technology Support Program of Jiangsu Province (BE2014389), the Jiangsu Provincial Key Laboratory of Agricultural Biology Open Fund (4911404215Z011) and the Jiangsu Collaborative Innovation Center for Modern Crop Production.

References

  1. Blumwald E, Poole RJ (1987) Salt tolerance in suspension cultures of sugar beet: induction of Na/H antiport activity at the tonoplast by growth in salt. Plant Physiol 83:884–887CrossRefGoogle Scholar
  2. Bradford MMA (1976) A rapid and sensitive method for the quantitation on microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  3. Ciniglia C, Mastrobuoni F, Scortichini M, Petriccione M (2015) Oxidative damage and cell–programmed death induced in Zea mays L by allelochemical stress. Ecotoxicology 24:926–937CrossRefGoogle Scholar
  4. Costantini P, Chernyak BV, Petronilli V, Bernardi P (1996) Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J Biol Chem 271:6746–6751CrossRefGoogle Scholar
  5. Cui X, Dong Y, Gi P, Wang H, Xu K, Zhang Z (2016) Relationship between root vigour, photosynthesis and biomass in soybean cultivars during 87 years of genetic improvement in the northern China. Photosynthetica 54:81–86CrossRefGoogle Scholar
  6. De Marchi U, Campello S, Szabò I, Tombola F, Martinou JC, Zoratti M (2004) Bax does not directly participate in the Ca2+—induced permeability transition of isolated mitochondria. J Biol Chem 279:37415–37422CrossRefGoogle Scholar
  7. Gao XB, Zhao FX, Xiang S, Hu YL, Hao YH, Su LT, Yang SQ, Mao ZQ (2010) Effects of cinnamon acid on respiratory rate and its related enzymes activity in roots of seedlings of malus hupehensis rehd. J Integ Agr 9:833–839Google Scholar
  8. Garofalo T, Manganelli V, Grasso M, Mattei V, Ferri A, Misasi R, Sorice M (2015) Role of mitochondrial raft–like microdomains in the regulation of cell apoptosis. Apoptosis 20:621–634CrossRefGoogle Scholar
  9. Gu Y, Chang ZZ, Yu JG, Zong LG (2013) Allelopathic effects of exogenous phenolic acids composted by wheat straw on seed germination and seedling growth of rice. Jiangsu J Agr Sci 29:240–246 (In Chinese)Google Scholar
  10. Hejl AM, Koster KL (2004) The allelochemical sorgoleone inhibits root H+–ATPase and water uptake. J Chem Ecol 30:2181–2191CrossRefGoogle Scholar
  11. Huang WJ, Oo TL, He HY, Wang AQ, Zhan J, Li CZ, Wei SQ, He LF (2014) Aluminum induces rapidly mitochondria–dependent programmed cell death in al–sensitive peanut root tips. Bot Stud 55:67–78CrossRefGoogle Scholar
  12. Huang W, Yang X, Yao S, Oo TL, He H, Wang A, Li C, He L (2014) Reactive oxygen species burst induced by aluminum stress triggers mitochondria–dependent programmed cell death in peanut root tip cells. Plant Physiol Bioc 82:76–84CrossRefGoogle Scholar
  13. Iversen CM (2014) Using root form to improve our understanding of root function. New Phytol 203:707–709CrossRefGoogle Scholar
  14. Jiang GY, Liu JG, Li YB (2015) Allelochemicals from cotton (Gossypium hirsutum) rhizosphere soil: inhibitory effects on cotton seedlings. Allelopathy J 35:153–162Google Scholar
  15. Jing F, Kang Y, Tan J, Tian B, Ma F, Liu J (2016) Decomposition characteristics of cotton stalks from fall to spring as affected by continuous cropping. Acta Agr Scand B S Plant 66:1–6Google Scholar
  16. Jung B, Alsanius BW, Jensén P (2001) Effects of some plant and microbial metabolites on germination and emergence of tomato seedlings. Acta Hort 548:603–609CrossRefGoogle Scholar
  17. Li M, Xia T, Jiang CS, Li LJ, Fu JL, Zhou ZC (2003) Cadmium directly induced the opening of membrane permeability pore of mitochondria which possibly involved in cadmium–triggered apoptosis. Toxicol 194:19–33CrossRefGoogle Scholar
  18. Li YB, Liu JG, Cheng XR, ZhangW Sun YY (2009) The allelopathic effects of returning cotton stalk to soil on the growth of succeeding cotton. Acta Ecol Sin 29:4942–4948 (in Chinese) Google Scholar
  19. Li Y, Allen VG, Chen J, Hou F, Brown CP, Green P (2013) Allelopathic influence of a wheat or rye cover crop on growth and yield of no–till cotton. Agron J 105:581–1587Google Scholar
  20. Lin J, Wang Y, Wang G (2005) Salt stress–induced programmed cell death via Ca2+–mediated mitochondrial permeability transition in tobacco protoplasts. Plant Growth Regu 45:243–250CrossRefGoogle Scholar
  21. Liu JG, Jiang GY, Bian XM, Li F, Geng W (2008) Allelopathic effects of cotton in continuous cropping. Allelopathy J 21:299–306Google Scholar
  22. Liu RX, Zhou ZG, Guo WQ, Chen BL, Oosterhuis DM (2008) Effects of N fertilization on root development and activity of water–stressed cotton (gossypium hirsutum L) plants. Agr Water Manage 95:1261–1270CrossRefGoogle Scholar
  23. Liu A, Chen S, Chang R, Liu D, Chen H, Ahammed GL, He C (2014) Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H2O2 accumulation and ATPase activity. J Plant Res 127:775–785CrossRefGoogle Scholar
  24. Mandhania S, Mandas S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biol Plantarum 50:227–231CrossRefGoogle Scholar
  25. Muriel P, Pérezrojas JM (2015) Nitric oxide inhibits mitochondrial monoamine oxidase activity and decreases outer mitochondria membrane fluidity. Comp Biochem Phys C 136:191–197Google Scholar
  26. Norberg E, Orrenius S, Zhivotovsky B (2010) Mitochondrial regulation of cell death: Processing of apoptosis–inducing factor (AIF). Biochem Bioph Res Co 396:95–100CrossRefGoogle Scholar
  27. Paillard M, Gomez L, Augeul L, Loufouat J, Lesnefsky EJ, Ovize M (2009) Postconditioning inhibits mPTP opening independent of oxidative phosphorylation and membrane potential. J Mol Cell Cardiol 46(6):902–909CrossRefGoogle Scholar
  28. Panda SK, Yamamoto Y, Kondo H, Matsumoto H (2008) Mitochondrial alterations related to programmed cell death in tobacco cells under aluminium stress. Compt Rend Biol 331:597–610CrossRefGoogle Scholar
  29. Rodriguez-Enriquez S, He L, Lemasters JJ (2004) Role of mitochondrial permeability transition pores in mitochondrial autophagy. Int J Biochem Cell Biol 36:2463–2472CrossRefGoogle Scholar
  30. Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29CrossRefGoogle Scholar
  31. Sui N, Zhou ZG, Yu CR, liu RX, Yang CQ, Zhang F, Song GL, Meng YL, (2015) Yield and potassium use efficiency of cotton with wheat straw incorporation and potassium fertilization on soils with various conditions in the wheat–cotton rotation system. Field Crops Res 172:132–144CrossRefGoogle Scholar
  32. Sun WX, Zheng HY, Lan J (2015) Edaravone protects osteoblastic cells from dexamethasone through inhibiting oxidative stress and mPTP opening. Mol Cell Biochem 409:1–8CrossRefGoogle Scholar
  33. Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D (2008) Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post–anthesis waterlogging. Photosynthetica 46:21–27CrossRefGoogle Scholar
  34. Tian G, Bi Y, Sun Z, Zhang L (2015) Phenolic acids in the plow layer soil of strawberry fields and their effects on the occurrence of strawberry anthracnose. Eur Journal Plant Pathol 143:1–14CrossRefGoogle Scholar
  35. Tonshin AA, Saprunova VB, Solodovnikova IM, Bakeeva LE, Yaguzhinsky LS (2003) Functional activity and ultrastructure of mitochondria isolated from myocardial apoptotic tissue. Biochemistry-Moscow  68:875–881Google Scholar
  36. Tsai CW, Lin CY, Lin HH, Chen JH (2011) Carnosic acid, a rosemary phenolic compound, induces apoptosis through reactive oxygen species–mediated p38 activation in human neuroblastoma IMR–32 cells. Neurochem Res 36:2442–2451CrossRefGoogle Scholar
  37. Vaughan D, Ord B (1990) Influence of phenolic acids on morphological changes in roots of Pisum sativum. J Sci Food Agr 52:289–299CrossRefGoogle Scholar
  38. Wang QQ, Hu YL, Zhou H, Zhan X, Mao ZQ (2012) Effects of phloridzin on the tricarboxylic acid cycle enzymes of roots of Malus hupehensis Rehd. Sci Agr Sin 45:3108–3114 (In Chinese)Google Scholar
  39. Xu ZY, Zheng MX, Zhang Y, Cui XZ, Yang SS, Liu RL, Li S, Lv QH, Zhao WL, Bai R (2016) The effect of the mitochondrial permeability transition pore on apoptosis in Eimeria tenella host cells. Poult Sci 95:2405–2413CrossRefGoogle Scholar
  40. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2003) Oxidative stress triggered by aluminum in plant roots. Plant Soil 255:239–243CrossRefGoogle Scholar
  41. Yao TT, Zhu LQ, Yang S, Zhou J, Zhu SH (2010) Effect of NO on oxidative damage to mitochondrial membrane in harvested plum fruit. Sci Agric Sin 43:2767–2774 (in Chinese) Google Scholar
  42. Zeng RN, Luo SM, Shi YH, Shi MB, Tu CY (2001) Physiological and biochemical mechanism of allelopathy of secalonic acid F on higher plants. Agron J 93:72–79CrossRefGoogle Scholar
  43. Zhao Y, Pan Z, Zhang Y, Qu X, Zhang Y, Yang Y, Jiang X, Huang S, Yuan M, Schumaker KS, Guo Y (2013) The actin–related protein2/3 complex regulates mitochondrial–associated calcium signaling during salt stress in arabidopsis. Plant Cell 25:4544–4559CrossRefGoogle Scholar
  44. Zhou J, Luan W, Huang XT, Qu HH, Ma DW, Zhang H (2016) Effect of Aqueous Extract of Galinsoga parviflora Cav.on Guard Cells of Vicia faba L. Southwest China J Agr Sci 29:800–804 (In Chinese)Google Scholar
  45. Zhu Y, Xu H, Huang K (2002) Mitochondrial permeabiltiy transition and cytochrome release induced by selenite. J Inorg Biochem 90:43–50CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.Key Laboratory of Cotton and Rape in Lower Reaches of Yangtze River of Ministry of Agriculture, Institute of Industrial CropsJiangsu Academy of Agricultural SciencesNanjingPeople’s Republic of China
  2. 2.Provincial Key Laboratory of Agrobiology/Jiangsu Academy of Agricultural SciencesNanjingPeople’s Republic of China

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