Skip to main content
SpringerLink
Log in

Effects of waterlogging on amyloplasts and programmed cell death in endosperm cells of Triticum aestivum L.

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The effects of waterlogging on amyloplasts and programmed cell death (PCD) in endosperm cells in Chinese wheat (Triticum aestivum L.; cv: Hua mai 8) are here discussed. Four water treatments were established from anthesis to maturity: they were 3 days of waterlogging treatment (DWT), 7 DWT, 12 DWT, and moderate water supply (the control). Lugol staining and scanning electron microscopy showed decreases in the number of amyloplasts and partially filled circular cavities under the waterlogging treatments. These resulted in serious deformities in the endosperm cells. Evans blue staining analysis and terminal deoxynucleotidyl transferase-mediated fluorescein deoxyuridine triphosphate nick-end labeling assays indicated that the PCD progression of endosperm cells occurred earlier under waterlogging treatments than in the control, so did the internucleosomal DNA fragmentation, which accompanies PCD in endosperm cells. Electron transmission microscopy analysis showed similar results. Under waterlogging treatments, the following PCD characteristics appeared earlier and were more pronounced than in normal endosperm cells: chromatin condensation, degradation of the nuclear envelope, swelling, and degradation of the mitochondrial cristae. Our study concluded that under waterlogging conditions, the number of amyloplasts tended to decrease and PCD was likely to appear ahead of time.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

DPA:

Days post anthesis

DWT:

Days waterlogging treatment

PCD:

Programmed cell death

TUNEL:

Terminal deoxynucleotidyl transferase-mediated fluorescein deoxyuridine triphosphate nick-end labeling

ABA:

Abscisic acid

WT:

Waterlogging treatment

References

  • Ahmadi A, Baker DA (2001) The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regul 35:81–91

    Article  CAS  Google Scholar 

  • Artlip TS, Madison JT, Setter TL (1995) Water deficit in developing endosperm of maize: cell division and nuclear DNA endoreduplication. Plant Cell Environ 18:1034–1040

    Article  CAS  Google Scholar 

  • Baruch DW, Meredith P, Jenkins LD, Simmons LD (1979) Starch granules of developing wheat kernels. Cereal Chem 56:554–558

    Google Scholar 

  • Bradford KJ, Yang SF (1980) Stress-induced ethylene production in the ethylene-requiring tomato mutant diageotropica. Plant Physiol 65:327–330

    Article  PubMed  CAS  Google Scholar 

  • Briarty LG, Hughes CE, Evers AD (1979) The developing endosperm of wheat: a stereological analysis. Ann Bot 44:641–658

    Google Scholar 

  • Brooks A, Jenner CF, Aspinall D (1982) Effects of water deficit on endosperm starch granules and on grain physiology of wheat and barley. Funct Plant Biol 9:423–436

    Google Scholar 

  • Buckner B, Johal GS, Buckner DJ (2000) Cell death in maize. Physiol Plantarum 108:231–239

    Article  CAS  Google Scholar 

  • Buttrose MS (1960) Submicroscopic development and structure of starch granules in cereal endosperms. J Ultra Res 4:231–257

    Article  CAS  Google Scholar 

  • Canetti L, Lomaniec E, Elkind Y, Lers A (2002) Nuclease activities associated with dark-induced and natural leaf senescence in parsley. Plant Sci 163:873–880

    Article  CAS  Google Scholar 

  • Cannell RQ, Belford RK, Gales K, Thomson RJ, Webster CP (1984) Effects of waterlogging and drought on winter wheat and winter barley grown on a clay and a sandy loam soil, crop growth and yield. Plant Soil 80:53–66

    Article  Google Scholar 

  • Cochrane MP, Paterson L, Duffus CM (1996) The effect of temperature on grain development and starch quality in barley. Aspects Appl Biol 45:139–146

    Google Scholar 

  • Demason DA (1994) Controls of germination in non-cereal monocotyledons. Advanced structure biology 3:285–310

    Google Scholar 

  • Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K + −efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479

    Article  PubMed  CAS  Google Scholar 

  • Deng XY, Li JW, Zhou ZQ, Fan HY (2010) Cell death in wheat roots induced by the powdery mildew fungus Blumeria graminis f. sp. Tritici. Plant Soil 328:45–55

    Article  CAS  Google Scholar 

  • Dengate H, Meredith P (1984) Variation in size distribution of starch granules form wheat grain. J Cereal Sci 2:83–90

    Article  Google Scholar 

  • Dominguez F, Moreno J, Cejudo FJ (2001) The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta 213:352–360

    Article  PubMed  CAS  Google Scholar 

  • Drew MC, Jackson MB, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive response to flooding in Zea mays L. Planta 147:83–88

    Article  CAS  Google Scholar 

  • Duffus CM (1992) Control of starch biosynthesis in developing cereal grains. Biochem Soc T 20:13–18

    CAS  Google Scholar 

  • Fukuda H (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Biol 44:245–253

    Article  PubMed  CAS  Google Scholar 

  • Gaffal KP, Friedrichs GJ, Gammal SE (2007) Ultrastructural evidence for a dual function of the phloem and programmed cell death in the floral nectary of Digitalis purpurea. Ann Bot 99:593–607

    Article  PubMed  Google Scholar 

  • Gallie DR, Young TE (2004) The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize. Mol Genet Genomics 271:267–281

    Article  PubMed  CAS  Google Scholar 

  • Greenberg JT, Guo A, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563

    Article  PubMed  CAS  Google Scholar 

  • Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214

    Article  PubMed  CAS  Google Scholar 

  • Guo B, Liang YC, Zhu YG (2009) Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? Plant Physiol 166:20–31

    Article  CAS  Google Scholar 

  • He CJ, Morgan PW, Drew MC (1996) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol 112:463–472

    PubMed  CAS  Google Scholar 

  • Hiron RWP, Wright STC (1973) The role of endogenous abscisic acid in the response of plants to stress. J Exp Bot 24:769–781

    Article  CAS  Google Scholar 

  • Kubo K, Shimazaki Y, Kobayashi H, Oyanagi (2007) A Specific variation in shoot growth and root traits under waterlogging conditions of the seedlings of Tribe Triticeae including Mizutakamoji (Agropyron humidum). Plant Prod Sci 10:91–98

    Article  Google Scholar 

  • Lam E, Pontier D, del Pozo O (1999) Die and let live—programmed cell death in plants. Curr Opin Plant Biol 2:502–507

    Article  PubMed  CAS  Google Scholar 

  • Langeveld SMJ, Wijk RV, Stuurman N, Kijine JW, Pater SD (2000) B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. J Exp Bot 51:1357–1361

    Article  PubMed  CAS  Google Scholar 

  • Li R, Lan SY, Xu ZX (2004) Programmed cell death in wheat during starchy endosperm development. J Plant physiol Mol Biol 30:183–188

    Google Scholar 

  • Liu SH, Fu BY, Xu HX, Zhu LH, Zha HQ, Li ZK (2007) Cell death in response to osmotic and salt stresses in two rice (Oryza sativa L.) ecotypes. Plant Sci 172:897–902

    Article  CAS  Google Scholar 

  • Mittler R, Simon L, Lam E (1997) Pathogen-induced programmed cell death in tobacco. J Cell Sci 110:1333–1344

    PubMed  CAS  Google Scholar 

  • Musgrave ME (1994) Waterlogging effects on yield and photosynthesis in eight winter wheat cultivars. Crop Sci 34:1314–1318

    Article  Google Scholar 

  • Nicolas M, Gleadow R, Dalling MJ (1985) Effect of post-anthesis drought on cell division and starch accumulation in developing wheat grains. Ann Bot 55:433–444

    Google Scholar 

  • Parker ML (1985) The relationship between A-type and B-type starch granules in the developing endosperm of wheat. J Cereal Sci 3:271–278

    Article  Google Scholar 

  • Peng M, Gao M, Abdel-Aal ESM, Hucl P, Chibbar RN (1999) Separation and characterization of A- and B-type starch granules in wheat endosperm. Cereal Chem 76:375–379

    Article  CAS  Google Scholar 

  • Pociecha E, Koscielniak J, Filek W (2008) Effects of root flooding and stage of development on the growth and photosynthesis of field bean (Vicia faba L. minor). Acta Physiol Plant 30:529–535

    Article  CAS  Google Scholar 

  • Setter TL, Flannigan BA (2001) Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J Exp Bot 52:1401–1408

    Article  PubMed  CAS  Google Scholar 

  • Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol 190:289–298

    Article  PubMed  CAS  Google Scholar 

  • Sharma DB, Swarup A (1988) Effects of short-term flooding on growth, yield and mineral of composition of wheat on sodic soil under field conditions. Plant Soil 107:137–143

    Article  CAS  Google Scholar 

  • Singh S, Singh G, Singh P, Singh N (2008) Effect of water stress at different stages of grain development on the characteristics of starch and protein of different wheat varieties. Food Chem 108:130–139

    Article  CAS  Google Scholar 

  • Smethurst CF, Shabala S (2003) Screening methods for water-logging tolerance in lucerne: comparative analysis of waterlogging effects on chlorophyll fluorescence, photosynthesis, biomass and chlorophyll content. Funct Plant Biol 30:335–343

    Article  Google Scholar 

  • Soulaka AB, Morrison WR (1985) The amylose and lipid contents, dimensions, and gelatinisation characteristics of some wheat starches and their A- and B-granule fractions. J Sci Food Agr 36:709–718

    Article  CAS  Google Scholar 

  • Tester RF, South JB, Morrison WR, Ellis RP (1991) The effects of ambient temperature during the grainfilling period on the composition and properties of starch form four barley genotypes. J Cereal Sci 13:113–127

    Article  CAS  Google Scholar 

  • van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LAJ, Petersen M, Smertenko A, Taliansky M, van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246

    Article  PubMed  Google Scholar 

  • Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytol 170:213–226

    Article  PubMed  CAS  Google Scholar 

  • Wang LK, Zhou ZQ, Song XF, Li JW, Deng XY, Mei FZ (2008) Evidence of ceased programmed cell death in metaphloem sieve elements in the development caryopsis of Triticum aestivum L. Protoplasma 234:87–96

    Article  PubMed  Google Scholar 

  • Wojciechowska M, Olszewska MJ (2003) Endosperm degradation during seed development of Echinocystis lobata (Cucurbitaceae) as a manifestation of programmed cell death (PCD) in plants. Folia Histochem Cyto 41:41–50

    Google Scholar 

  • Young TE, Gallie DR (1999) Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals. Plant Mol Biol 39:915–926

    Article  PubMed  CAS  Google Scholar 

  • Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301

    Article  PubMed  CAS  Google Scholar 

  • Young TE, Callie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751

    PubMed  CAS  Google Scholar 

  • Zhang J (2008) Studies on the degeneration of nucleus and cytoplasm development during the PCD progresses of starch endosperm in Triticeae crops. MA dissertation of Yangzhou University (article in Chinese)

  • Zhao J (1995) Physical geography of China, 3rd edn, BeiJing (article in Chinese)

  • Zhao H, Dai TB, Jiang D, Jing Q, CAO WX (2007) Effects of drought and waterlogging on flag leaf post-anthesis photosynthetic characteristics and assimilates translocation in winter wheat under high temperature. Ying Yong Sheng Tai Xue Bao 18:333–338

    PubMed  Google Scholar 

  • Zhou ZQ, Wang LK, Li JW, Song XF, Yang CN (2008) Study on programmed cell death and dynamic changes of starch accumulation in pericarp cells of Triticum aestivum L. Protoplasma 236:49–58

    Article  Google Scholar 

  • Zuppini A, Navazio L, Sella L, Castiglioni C, Favaron F, Mariani P (2005) An endopolygalacturonase from Sclerotinia sclerotiorum induces calcium-mediated signaling and programmed cell death in soybean cells. Mol Plant-Microbe Interac 18:849–855

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work is supported by the National Natural Science Foundation of China (grant nos. 31071347 and 31171469).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Laboratory of Cell Biology, Huazhong Agricultural University, Wuhan, 430070, China

    Hai-Yan Fan, Zhu-Qing Zhou, Chao-Nan Yang, Zhen Jiang, Xiang-Xu Cheng & Yue-Jing Guo

  2. National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, 430070, China

    Jin-Tao Li

  3. Huazhong Agricultural University, Wuhan, 430070, China

    Jin-Tao Li

  4. College of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Hai-Yan Fan, Zhu-Qing Zhou, Chao-Nan Yang, Zhen Jiang, Xiang-Xu Cheng & Yue-Jing Guo

Authors
  1. Hai-Yan Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhu-Qing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chao-Nan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhen Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jin-Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiang-Xu Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yue-Jing Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhu-Qing Zhou.

Additional information

Handling Editor: Peter Nick

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 16 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fan, HY., Zhou, ZQ., Yang, CN. et al. Effects of waterlogging on amyloplasts and programmed cell death in endosperm cells of Triticum aestivum L.. Protoplasma 250, 1091–1103 (2013). https://doi.org/10.1007/s00709-013-0485-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-013-0485-z

Keywords

Search

Navigation