Skip to main content
SpringerLink
Log in

Short-term waterlogging-induced autophagy in root cells of wheat can inhibit programmed cell death

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

Abstract

Autophagy is a pathway for the degradation of cytoplasmic components in eukaryotes. In wheat, the mechanism by which autophagy regulates programmed cell death (PCD) is unknown. Here, we demonstrated that short-term waterlogging-induced autophagy inhibited PCD in root cells of wheat. The waterlogging-tolerant wheat cultivar Huamai 8 and the waterlogging-sensitive wheat cultivar Huamai 9 were used as experimental materials, and their roots were waterlogged for 0–48 h. Waterlogging stress increased the number of autophagic structures, the expression levels of autophagy-related genes (TaATG), and the occurrence of PCD in root cells. PCD manifested as morphological changes in the cell nucleus, significant enhancement of DNA laddering bands, and increases in caspase-like protease activity and the expression levels of metacaspase genes. The autophagy promoter rapamycin (RAPA) reduced PCD levels, whereas the autophagy inhibitor 3-methyladenine (3-MA) enhanced them. The expression levels of TaATG genes and the number of autophagic structures were lower in cortex cells than in stele cells, but the levels of PCD were higher in cortex cells. The number of autophagic structures was greater in Huamai 8 than in Huamai 9, but the levels of PCD were lower. In summary, our results showed that short-term waterlogging induced autophagy which could inhibit PCD. Mechanisms of response to waterlogging stress differed between cortex and stele cells and between two wheat cultivars of contrasting waterlogging tolerance.

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

Similar content being viewed by others

Abbreviations

ATG:

Autophagy-related gene

DAPI:

4′,6-Diamidino-2-phenylindole

PCD:

Programmed cell death

RAPA:

Rapamycin

ROS:

Reactive oxygen species

3-MA:

3-Methyladenine

References

  • Baehrecke EH (2002) How death shapes life during development. Nat Rev Mol Cell Biol 3:779–787

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138

    Article  CAS  PubMed  Google Scholar 

  • Cai YM, Yu J, Gallois P (2014) Endoplasmic reticulum stress-induced PCD and caspase-like activities involved. Front Plant Sci 5:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai YM, Yu J, Ge Y, Mironov A, Gallois P (2018) Two proteases with caspase-3-like activity, cathepsin B and proteasome, antagonistically control ER-stress-induced programmed cell death in Arabidopsis. New Phytol 218:1143–1155

  • Chen Y, Chen X, Wang HJ, Bao YQ, Zhang W (2014) Examination of the leaf proteome during flooding stress and the induction of programmed cell death in maize. Proteome Sci 12(1):33

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen L, Liao B, Qi H, Xie LJ, Huang L, Tian WJ, Zhai N, Yuan LB et al (2015) Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana. Autophagy 11:12.2233–12.2246

    Article  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 

  • Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F, Dangl JL, Epple P (2010) Arabidopsis type I metacaspases control cell death. Science 330:1393–1397

    Article  CAS  PubMed  Google Scholar 

  • Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. J Exp Bot 62:39–57

    Article  CAS  PubMed  Google Scholar 

  • Cui J, Chen B, Wang H, Han Y, Chen Y, Zhang W (2016) Glucosidase II β-subunit, a novel substrate for caspase-3-like activity in rice, plays as a molecular switch between autophagy and programmed cell death. Sci Rep 6:31764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dauphinee AN, Fletcher JI, Denbigh GL, Lacroix CR, Gunawardena AHLAN (2017) Remodelling of lace plant leaves: antioxidants and ROS are key regulators of programmed cell death. Planta 246(1):133–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dauphinee AN, Denbigh GL, Rollini A, Fraser M, Lacroix CR, Gunawardena AHLAN (2019) The function of autophagy in lace plant programmed cell death. Front Plant Sci 10:1198

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng XY, Li JW, Yang CN, Jiang Z, Xiao SX, Zhou ZQ (2009) A preliminary study on PCD aspects and roles of reactive oxygen species during Aerenchyma formation in wheat roots under waterlogging. J Triticeae Crops 29(5):832–838

    CAS  Google Scholar 

  • Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127

    Article  CAS  PubMed  Google Scholar 

  • Duan Y, Zhang W, Li B, Wang Y, Li K, Sodmergen HC, Zhang Y, Li X (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytol 186:681–695

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms:signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  CAS  PubMed  Google Scholar 

  • Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147(4):742–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallois P (2016) Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis. Cell Death Differ 23:1493–1501

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao JF (2006) Experimental guidance for plant physiology. Higher Education Press, Beijing in Chinese

    Google Scholar 

  • Ge Y, Cai YM, Bonneau L, Rotari V, Danon A, McKenzie EA, McLellan H, Mach L, Gallois P (2016) Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis. Cell Death Differ 23(9):1493–1501

  • Gladish, D. K., Xu, J., & Niki, T. (2006). Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Annals of botany, 97(5):895–902

  • Gill MB, Zeng FR, Shabala L, Zhang G, Yu M et al (2019) Identifification of QTL related to ROS formation under hypoxia and their association with waterlogging and salt tolerance in barley. Int J Mol Sci 20(3):669

    Article  Google Scholar 

  • Guan B, Lin Z, Liu D, Li CY, Zhou ZQ, Mei F, Li J, Deng X (2019) Effect of waterlogging-induced autophagy on programmed cell death in Arabidopsis roots. Front Plant Sci 10:468

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao Y, Wang X, Wang K, Li H, Duan X, Tang C, Kang Z (2016) TaMCA1, a regulator of cell death, is important for the interaction between wheat and Puccinia striiformis. Sci Rep 6:26946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herzog M, Striker GG, Colmer TD, Pedersen O (2016) Mechanisms of waterlogging tolerance in wheat-a review of root and shoot physiology. Plant Cell Environ 39:1068–1086

    Article  CAS  PubMed  Google Scholar 

  • Jiang Z, Song XF, Zhou ZQ, Wang LK, Li JW, Deng XY, Fan HY (2010) Aerenchyma formation: programmed cell death in adventitious roots of winter wheat (Triticum aestivum L.) under waterlogging. Funct Plant Biol 37(8):748–755

    Article  Google Scholar 

  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ et al (2016) Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12(1):1–222

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurusu T, Higaki T, Kuchitsu K (2015) Programmed cell death in plant immunity: cellular reorganization, signaling, and cell cycle dependence in cultured cells as a model system. Plant programmed cell death. Springer, Chap 4, pp 77–96

  • Li YB, Cui DZ, Sui XX, Huang C, Huang CY, Fan QQ, Chu XS (2019) Autophagic survival precedes programmed cell death in wheat seedlings exposed to drought stress. Int J Mol Sci 20(22):5777

    Article  CAS  PubMed Central  Google Scholar 

  • Lin Z (2019) Effects of ROS accumulation on autophagy level of wheat root cells during the formation of aerenchyma under waterlogging stress. Huazhong Agricultural University, Wuhan

    Google Scholar 

  • Liu X (2010) Cloning of wheat autophagy related genes and functional analysis of TaATG6 and TaATG3 genes. Northwest A&F University, YangLing

    Google Scholar 

  • Loreti E, Van Veen H, Perata P (2016) Plant responses to flooding stress. Curr Opin Plant Biol 33:64–71

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Zhang P, Zhu R, Fu J, Su J, Zheng J, Wang Z, Wang D, Gong Q (2017) Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci 8:1459

    Article  PubMed  PubMed Central  Google Scholar 

  • Michaeli S, Galili G, Genschik P, Fernie AR, Avin-Wittenberg T (2016) Autophagy in plants-what’s new on the menu? Trends Plant Sci 21(2):134–144

    Article  CAS  PubMed  Google Scholar 

  • Minina EA, Bozhkov PV, Hofius D (2014) Autophagy as initiator or executioner of cell death. Trends Plant Sci 19:692–697

    Article  CAS  PubMed  Google Scholar 

  • Nair U, Yen WL, Mari M, Cao Y, Xie Z, Baba M, Reggiori F, Klionsky DJ (2012) A role for Atg8–PE deconjugation in autophagosome biogenesis. Autophagy 8(5):780–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakaune S, Yamada K, Kondo M, Kato T, Tabata S, Nishimura M, Hara-Nishimura I (2005) A vacuolar processing enzyme, dVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17:876–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navarro-Yepes J, Burns M, Anandhan A, Khalimonchuk O, del Razo LM, Quintanilla-Vega B, Pappa A, Panayiotidis MI, Franco R (2014) Oxidative stress, redox signaling, and autophagy: cell death versus survival. Antioxid Redox Signal 21(1):66–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ploschuk RA, Miralles DJ, Colmer TD, Ploschuk EL, Striker GG (2018) Waterlogging of winter crops at early and late stages: impacts on leaf physiology, growth and yield. Front Plant Sci 9:1863

    Article  PubMed  PubMed Central  Google Scholar 

  • Qi X, Li Q, Ma X, Qian C et al (2018) Waterlogging-induced adventitious root formation in cucumber is regulated by ethylene and auxin through reactive oxygen species signalling. Plant Cell Environ 42(5):1458–1470

    Article  Google Scholar 

  • Qi YH, Mao FF, Zhou ZQ, Liu DC, Min-Yu, Deng XY, Li JW, Mei FZ (2019) The release of cytochrome c and the regulation of the programmed cell death progress in the endosperm of winter wheat (Triticum aestivum L.) under waterlogging. Protoplasma 255(6):1651–1665

  • Shibuya K, Yamada T, Ichimura K (2009) Autophagy regulates progression of programmed cell death during petal senescence in Japanese morning glory. Autophagy 5(4):546–547

    Article  CAS  PubMed  Google Scholar 

  • Song X, Wang L, Zhou Z (2009) Aerenchyma formation and the Ultrastructural changes of cortical cells in wheat roots under waterlogging. J Huazhong Agric Univ:519–524

  • Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 91:119–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Jia X, Huo L, Che R, Gong X, Wang P (2018) MdATG18a overexpression improves tolerance to nitrogen deficiency and regulates anthocyanin accumulation through increased autophagy in transgenic apple. Plant Cell Environ 41(2):469–480

    Article  CAS  PubMed  Google Scholar 

  • Takamitsu K, Kazuyuki K (2017) Autophagy, programmed cell death and reactive oxygen species in sexual reproduction in plants. J Plant Res 130:491–499

    Article  Google Scholar 

  • Topchieva LV, Nilova IA, Titov AF (2017) The level of proapoptotic gene transcripts in wheat leaves under high temperature stress. Dokl Biochem Biophys 472(1):5–8

    Article  CAS  PubMed  Google Scholar 

  • Tran V, Weier D, Radchuk R, Thiel J, Radchuk V (2014). Caspase-like activities accompany programmed cell death events in developing barley grains. PloS One 9(10):e109426

  • Üstün S, Hafrén A, Hofius D (2017) Autophagy as a mediator of life and death in plants. Curr Opin Plant Biol 40:122–130

    Article  PubMed  Google Scholar 

  • Van T, Diana W, Ruslana R et al (2014) Caspase-like activities accom- pany programmed cell death events in developing barley grains. PLoS One 9(10):e109426

  • Vera VS, Kenchappa CS, Landberg K et al (2017) Autophagy is required for gamete differentiation in the moss\r Physcomitrella patens. Autophagy 11:1939–1951

    Article  Google Scholar 

  • Wang X, Wang X, Feng H, Tang C, Bai P, Wei G, Huang L, Kang Z (2012) TaMCA4, a novel wheat Metacaspase gene functions in programmed cell death induced by the fungal pathogen Puccinia striiformis f. sp. tritici. Mol Plant-Microbe Interact 25(6):755–764

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zhao L, Hou H, Zhang H, Huang Y, Wang Y, Li H, Gao F, Yan S, Li L (2015) Epigenetic changes are associated with programmed cell death induced by heat stress in seedling leaves of Zea mays. Plant Cell Physiol 56(5):965–976

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Lam E (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J Biol Chem 283:3200–3210

    Article  CAS  PubMed  Google Scholar 

  • Xu Q (2013) Study on the establishment model and dynamic changes of aerenchyma in wheat roots. [D]. Library of Huazhong Agricultural University, Wuhan

    Google Scholar 

  • Xu J, Wu Y, Lu G, Xie S, Ma Z et al (2017) Importance of ROS-mediated autophagy in determining apoptotic cell death induced by physapubescin B. Redox.Biol 12:198–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken-2 genotypes. Plant Physiol 115:737–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yue J, Sun H, Zhang W, Pei D, He Y, Wang H (2015) Wheat homologs of yeast ATG6 function in autophagy and are implicated in powdery mildew immunity. BMC Plant Biol 15(1):95

    Article  PubMed  PubMed Central  Google Scholar 

  • Yue W, Nie X, Cui L, Zhi Y, Zhang T, du X, Song W (2018) Genome-wide sequence and expressional analysis of autophagy gene family in bread wheat (Triticum aestivum L.). J Plant Physiol 229:7–21

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Liu W, Kong L, Wang M (2008) Systemic PCD occurs in TMV-tomato interaction. Sci China C Life Sci 51(11):1009–1019

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Hong Q, Li Y, Li Q, Wang M (2018) Autophagy contributes to regulate the ROS levels and PCD progress in TMV-infected tomatoes. Plant Sci 269:12–19

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant No.31871530).

Author information

Authors and Affiliations

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

    Li-Lang Zhou, Kai-Yue Gao, Li-Sha Cheng, Yue-Li Wang, Yi-Keng Cheng, Qiu-Tao Xu & Zhu-Qing Zhou

  2. College of Food and Biological Science and Technology, Wuhan Institute of Design and Sciences, Wuhan, 430070, Hubei, China

    Xiang-Yi Deng & Ji-Wei Li

  3. College of Plant Sciences and Technology, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Fang-Zhu Mei

Authors
  1. Li-Lang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kai-Yue Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li-Sha Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yue-Li Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi-Keng Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qiu-Tao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiang-Yi Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ji-Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fang-Zhu Mei
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhu-Qing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhu-Qing Zhou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Néstor Carrillo

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 120 kb)

ESM 2

(DOCX 682 kb)

ESM 3

(DOCX 486 kb)

ESM 4

(DOCX 15.3 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, LL., Gao, KY., Cheng, LS. et al. Short-term waterlogging-induced autophagy in root cells of wheat can inhibit programmed cell death. Protoplasma 258, 891–904 (2021). https://doi.org/10.1007/s00709-021-01610-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-021-01610-8

Keywords

Search

Navigation