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Physiological mechanism of programmed cell death aggravation and acceleration in wheat endosperm cells caused by waterlogging

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Abstract

Wheat (Triticum aestivum L.) is one of the world’s three major food crops, the previous studies have indicated that the development of wheat endosperm cells underwent a special programmed cell death (PCD) and it could be accelerated by waterlogging. Hua 8 wheat cultivar (waterlogging tolerant) and Hua 9 (waterlogging sensitive) were used to reveal the physiological mechanism in this study. The results showed that after 7 days waterlogging treatment (DWT), the malondialdehyde (MDA) and O2 (superoxide anion-free radical) were increased in both endosperms, especially in Hua 9 endosperm. Content of hydrogen peroxide (H2O2) increased significantly in both endosperms at 12 days after flowering (DAF) and 15 DAF. Proline, soluble sugar, and protein contents in Hua 8 endosperm were increased, nevertheless, the soluble sugar and proline contents declined in Hua 9 endosperm. The activities of superoxide dismutase (SOD) were induced in both endosperms, especially in Hua 8, while showed different change trends in activities of peroxidase (POD) and catalase (CAT). The SOD isozyme spectrogram appeared a new band, and CAT added two bands in Hua 8 endosperm after 7 DWT. CAT isozyme activity was increased markedly, but SOD isozyme in Hua 9 endosperm showed no significant effect by waterlogging stress. Above all, the accumulation of MDA, O2 , and H2O2 in wheat endosperm after waterlogging led to the aggravation of PCD progress. Compared to Hua 8, more reactive oxygen species (ROS) accumulated in Hua 9 endosperm after waterlogging, combined with the weak ROS scavenging enzyme activities, in addition to the low osmotic pressure accelerated the PCD progress.

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References

  • Bano S, Ashraf M, Akram NA (2014) Salt stress regulates enzymatic and nonenzymatic antioxidative defense system in the edible part of carrot (Daucus carota L.). J Plant Interact 9:324–329

    Article  CAS  Google Scholar 

  • Bar NN, Poljakoff MA (1977) Salinity stress and the content of proline in roots of Pisum sativum and Tamarix tetragyna. Ann Bot Lond 41:173–179

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cheng XX, Yu M, Zhang N, Zhou ZQ, Xu QT, Mei FZ, Qu LH (2016) Reactive oxygen species regulate programmed cell death progress of endosperm in winter wheat (Triticum aestivum L.) under waterlogging. Protoplasma 253:311–327

    Article  CAS  PubMed  Google Scholar 

  • Das S, Krishnan P, Nayak M, Ramakrishnan B (2013) Changes in antioxidant isozymes as a biomarker for characterizing high temperature stress tolerance in rice (Oryza sativa L.) spikelets. Exp Agric 49:53–73

    Article  Google Scholar 

  • Deng B, Du W, Liu C, Sun W, Tian S, Dong H (2012) Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids? Plant Growth Regul 66:37–47

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith E (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Elslner EF (1982) Oxygen activation and oxygen toxicity. Annu Rev Plant Physiol 33:73–96

    Article  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

  • Fan HY, Zhou ZQ, Yang CN, Jiang Z, Li JT, Cheng XX, Guo YJ (2013) Effects of waterlogging on amyloplasts and programmed cell death in endosperm cells of Triticum aestivum L. Protoplasma 250:1091–1103

    Article  CAS  PubMed  Google Scholar 

  • Farooq M, Wahid A, Lee DJ, Cheema SA, Aziz T (2010) Comparative time course action of the foliar applied glycinebetaine, salicylic acid, nitrous oxide, brassinosteroids and spermine in improving drought resistance of rice. J Agron Crop Sci 196:336–345

    Article  CAS  Google Scholar 

  • Fielding JL, Hall JL (1978) A biolchemical and cytochemical study of peroxidase activity in roots of Pisum sativum. J Exp Bot 29:969–981

    Article  CAS  Google Scholar 

  • Gechev TS, Hille J (2006) Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 168:17–20

    Article  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goraya GK, Asthir B (2016) Magnificant role of intracellular reactive oxygen species production and its scavenging encompasses downstream processes. J Plant Biol 59:215–222

    Article  CAS  Google Scholar 

  • Habibzadeh F, Sorooshzadeh A, Pirdashti H, Modarres-Sanavy SAM (2013) Alleviation of waterlogging damage by foliar application of nitrogen compounds and tricyclazole in canola. Aust J Crop Sci 7:401–406

    CAS  Google Scholar 

  • Haddadi BS, Hassanpour H, Niknam V (2016) Effect of salinity and waterlogging on growth, anatomical and antioxidative responses in Mentha aquatica L. Acta Physiol Plant 38:1–11

    Article  CAS  Google Scholar 

  • Han Q, Kang G, Guo T (2013) Proteomic analysis of low temperature stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem 63:236–244

    Article  CAS  PubMed  Google Scholar 

  • Hautegem TV, Waters AJ, Goodrich J, Nowack MK (2015) Only in dying, life: programmed cell death during plant development. Trends Plant Sci 20:1360–1385

    Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359

    Google Scholar 

  • Hossain MA, Uddin SN (2011) Mechanisms of waterlogging tolerance in wheat: morphological and metabolic adaptations under hypoxia or anoxia. Aust J Crop Sci 5:1094–1101

    CAS  Google Scholar 

  • Islam MA, Macdonald SE (2004) Ecophysiological adaptations of black spruce (Picea mariana) and tamarack (Laris laricina) seedlings to flooding. Trees 18:35–42

    Article  Google Scholar 

  • Jing YP, Liu DT, Xu XR, Xiong F, Li LD, Zheng YK, Hao YF, Gu YJ, Wang Z (2014) Development of endosperm cells and starch granules in common wheat. Cereal Res Commun 42:514–524

    Article  Google Scholar 

  • Kaur G, Singh HP, Batish DR, Kohli RK (2013) Lead (Pb)-induced biochemical and ultrastructural changes in wheat (Triticum aestivum) roots. Protoplasma 250:53–62

    Article  CAS  PubMed  Google Scholar 

  • Kaur R, Gupta AK, Taggar GK (2014) Role of catalase, H2O2 and phenolics in resistance of pigeonpea towards Helicoverpa armigera (Hubner). Acta Physiol Plant 36:1513–1527

    Article  CAS  Google Scholar 

  • Kraj W (2016) Reactive oxygen species and antioxidant levels as the factors of autumn senescence in phenological forms of beech (Fagus sylvatica L.). Acta Physiol Plant 38:1–12

    Article  CAS  Google Scholar 

  • Lee YH, Kim KS, Jang YS, Hwang JH, Lee DH, Choi IH (2014) Global gene expression responses to waterlogging in leaves of rape seedlings. Plant Cell Rep 33:289–299

    Article  CAS  PubMed  Google Scholar 

  • Liu MX, Jiang YW (2015) Genotypic variation in growth and metabolic responses of perennial ryegrass exposed to short-term waterlogging and submergence stress. Plant Physiol Biochem 95:57–64

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Wang Y, Pan K, Li W, Zhang L, Shen X, Liu L, Deng M (2014) Responses of antioxidant defense system to drought stress in the leaves of Fargesia denudata seedlings, the staple food on the giant panda. Russ J Plant Physl +3:374–383

  • Manaa A, Mimounia H, Terrasa A, Chebila F, Wastia S, Gharbib E, Ahmed HB (2014) Superoxide dismutase isozyme activity and antioxidant responses of hydroponically cultured Lepidium sativum L. to NaCl stress. J Plant Interact 9:440–449

    Article  CAS  Google Scholar 

  • Meng Y, Di B, Zhang G, Feng XG, Xu CL, Tian J (2013) The correlation analysis of soluble sugar and starch contents with electrical impedance in Betula platyphylla suk. roots under waterlogging and flooding stresses. Acta Bioph Sin 29:450–460 (in Chinese)

    Article  CAS  Google Scholar 

  • Mueller S, Riedel HD, Stremmel W (1997) Determination of catalase activity at physiological hydrogen peroxide concentrations. Anal Biochem 245:55–60

    Article  CAS  PubMed  Google Scholar 

  • Najeeb U, Bange MP, Atwell BJ, Tan DKY (2016) Low incident light combined with partial waterlogging impairs photosynthesis and imposes a yield penalty in cotton. J Agron Crop Sci 202:331–341

    Article  CAS  Google Scholar 

  • Noreen Z, Ashraf M (2009) Assessment of variation in antioxidative defense system in salt-treated pea (Pisum sativum) cultivars and its putative use as salinity tolerance markers. J Plant Physiol 166:1764–1774

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  • Pucciariello C, Perata P (2016) New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants. Water Res 40:2246–2257

    Google Scholar 

  • Shaw RE, Meyer WS, McNeill A, Tyerman SD (2013) Waterlogging in Australian agricultural landscapes: a review of plant responses and crop models. Crop Pasture Sci 64:549–562

    Article  Google Scholar 

  • Tatar O, Gevrek MN (2008) Influence of water stress on proline accumulation, lipid peroxidation and water content of wheat. J Anim Sci 7:409–412

    CAS  Google Scholar 

  • Turkan I, Demiral T, Sekmen AH (2013) The regulation of antioxidant enzymes in two Plantago species differing in salinity tolerance under combination of waterlogging and salinity. Funct Plant Biol 40:484–493

    Article  CAS  Google Scholar 

  • Wang Y, Zheng XY, Yu BJ, Han SJ, Guo JB, Tang HP, Yu AYZL, Deng HT, Hong YG, Liu YL (2015) Disruption of microtubules in plants suppresses macroautophagy and triggers starch excess-associated chloroplast autophagy. Autophagy 11:2259–2274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia LJ, Yang LQ, Sun NL, Li J, Fang YJ, Wang YP (2016) Physiological and antioxidant enzyme gene expression analysis reveals the improved tolerance to drought stress of the somatic hybrid offspring of Brassica napus and Sinapis alba at vegetative stage. Acta Physiol Plant 38:1–10

    Article  Google Scholar 

  • Yin DM, Chen SM, Chen FD, Guan ZY, Fang WM (2010) Morpho-anatomical and physiological responses of two Dendranthema species to waterlogging. Environ Exp Bot 68:122–130

    Article  CAS  Google Scholar 

  • Zhang M, Fang Y, Ji Y, Jiang Z, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot 85:1–9

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Foundation of China (Grant Nos. 31171469 and 31471428). The author would like to acknowledge the anonymous reviewers for their valuable comments.

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Correspondence to Zhuqing Zhou.

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Communicated by J. Zwiazek.

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Yu, M., Zhou, Z., Deng, X. et al. Physiological mechanism of programmed cell death aggravation and acceleration in wheat endosperm cells caused by waterlogging. Acta Physiol Plant 39, 23 (2017). https://doi.org/10.1007/s11738-016-2324-2

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  • DOI: https://doi.org/10.1007/s11738-016-2324-2

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