Skip to main content
Log in

Differential cell persistence is observed in the Arabidopsis female gametophyte during heat stress

  • Short Communication
  • Published:
Plant Reproduction Aims and scope Submit manuscript

Abstract

Key message

The central cell withstands heat stress better than the egg and antipodal cells. Insilco analysis of transcriptomic data identified several heat responsive genes which are central cell specific.

Abstract

Crop damage due to heat stress (HS) is a major cause of yield lost. Plants are particularly susceptible to negative effects of HS during gametophyte development and fertilization. Extensive studies have been performed on the male gametophyte under HS, but how the female gametophyte copes with HS is largely unknown. To learn how the different cell types of the female gametophyte reacts to HS, we studied unfertilized CDC123::H2B:YFP ovules. We found that the YFP-specific florescent signal persisted in the central cell during HS significantly more than the egg cell. We also found that the fluorescent signal persistence was the lowest in the antipodal cells. This finding suggests that the reaction of the female gametophyte to HS is rather unique and differentially mediated according to the cell’s identity. In addition, mining through published transcriptomic datasets we found that several important heat stress responsive genes which are extremely upregulated during HS (more than 64-fold) are specifically expressed in the CC but not in the EC. Further research such as comparative transcriptomics and cell biology will likely shed more light on the phenomena reported here and increase our basic understandings about the ways sexual reproduction processes are affected by heat stress.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Ahammed GJ, Li X, Zhou J, Zhou YH, Yu JQ (2016) Role of hormones in plant adaptation to heat stress. In: Ahammed GJ, Yu J-Q (eds) Plant hormones under challenging environmental factors. Springer, Dordrecht, pp 1–21

    Google Scholar 

  • Ambastha V, Friedmann Y, Leshem Y (2020) Laterals take it better—emerging and young lateral roots survive lethal salinity longer than the primary root in Arabidopsis. Sci Rep 10:1–11

    Google Scholar 

  • Awasthi R, Bhandari K, Nayyar H (2015) Temperature stress and redox homeostasis in agricultural crops. Front Environ Sci 3:1–24

    Google Scholar 

  • Begcy K, Nosenko T, Zhou LZ, Fragner L, Weckwerth W, Dresselhaus T (2019) Male sterility in maize after transient heat stress during the tetrad stage of pollen development. Plant Physiol 181:683–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen T, Fluhr R (2018) Singlet oxygen plays an essential role in the root’s response to osmotic stress. Plant Physiol 177:1717–1727

    CAS  PubMed  PubMed Central  Google Scholar 

  • Christians ES, Zhou Q, Renard J, Benjamin IJ (2003) Heat shock proteins in mammalian development. Semin Cell Dev Biol 14:283–290

    CAS  PubMed  Google Scholar 

  • Deryng D, Conway D, Ramankutty N, Price J, Warren R (2014) Global crop yield response to extreme heat stress under multiple climate change futures. Environ Res Lett 9:041001

    Google Scholar 

  • Drews GN, Koltunow AMG (2011) The female gametophyte. Arabidopsis Book Am Soc Plant Biol 9:e0155

    Google Scholar 

  • Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao K, Liu YL, Li B, Zhou RG, Sun DY, Zheng SZ (2014) Arabidopsis thaliana phosphoinositide-specific phospholipase C isoform 3 (AtPLC3) and AtPLC9 have an additive effect on thermotolerance. Plant Cell Physiol 55:1873–1883

    CAS  PubMed  Google Scholar 

  • Giorno F, Wolters-Arts M, Mariani C, Rieu I (2013) Ensuring reproduction at high temperatures: the heat stress response during anther and pollen development. Plants 2:489–506

    PubMed  PubMed Central  Google Scholar 

  • Groß-Hardt R, Kägi C, Baumann N, Moore JM, Baskar R, Gagliano WB, Jürgens G, Grossniklaus U (2007) LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol 5:0494–0500

    Google Scholar 

  • Hedhly A (2011) Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ Exp Bot 74:9–16

    Google Scholar 

  • Jegadeesan S, Chaturvedi P, Ghatak A, Pressman E, Meir S, Faigenboim A, Rutley N, Beery A, Harel A, Weckwerth W et al (2018) Proteomics of heat-stress and ethylene-mediated thermotolerance mechanisms in tomato pollen grains. Front Plant Sci 871:1–20

    Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    CAS  PubMed  Google Scholar 

  • Lenzoni G, Knight MR (2019) Increases in absolute temperature stimulate free calcium concentration elevations in the chloroplast. Plant Cell Physiol 60:538–548

    CAS  PubMed  Google Scholar 

  • Liu Q, Yan S, Yang T, Zhang S, Chen YQ, Liu B (2017) Small RNAs in regulating temperature stress response in plants. J Integr Plant Biol 59:774–791

    CAS  PubMed  Google Scholar 

  • Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620

    CAS  PubMed  Google Scholar 

  • Lohani N, Singh MB, Bhalla PL (2020) High temperature susceptibility of sexual reproduction in crop plants (C Foyer, Ed.). J Exp Bot 71:555–568

    PubMed  Google Scholar 

  • Long SP, Ort DR (2010) More than taking the heat: crops and global change. Curr Opin Plant Biol 13:241–248

    PubMed  Google Scholar 

  • MacPhee DJ (ed) (2017) The role of heat shock proteins in reproductive system development and function. Springer, Cham

    Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125

    CAS  PubMed  Google Scholar 

  • Mora C, Dousset B, Caldwell IR, Powell FE, Geronimo RC, Bielecki CR, Counsell CWW, Dietrich BS, Johnston ET, Louis LV et al (2017) Global risk of deadly heat. Nat Clim Change 7:501–506

    Google Scholar 

  • Mora C, Spirandelli D, Franklin EC, Lynham J, Kantar MB, Miles W, Smith CZ, Freel K, Moy J, Louis LV et al (2018) Broad threat to humanity from cumulative climate hazards intensified by greenhouse gas emissions. Nat Clim Change 8:1062–1071

    CAS  Google Scholar 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65

    CAS  PubMed  Google Scholar 

  • Ozga JA, Kaur H, Savada RP, Reinecke DM (2017) Hormonal regulation of reproductive growth under normal and heat-stress conditions in legume and other model crop species. J Exp Bot 68:1885–1894

    CAS  PubMed  Google Scholar 

  • Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    CAS  PubMed  Google Scholar 

  • Rahmati Ishka M, Brown E, Weigand C, Tillett RL, Schlauch KA, Miller G, Harper JF (2018) A comparison of heat-stress transcriptome changes between wild-type Arabidopsis pollen and a heat-sensitive mutant harboring a knockout of cyclic nucleotide-gated cation channel 16 (cngc16). BMC Genom 19:1–19

    Google Scholar 

  • Rieu I, Twell D, Firon N (2017) Pollen development at high temperature: from acclimation to collapse. Plant Physiol 173:1967–1976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rupik W, Jasik K, Bembenek J, Widłak W (2011) The expression patterns of heat shock genes and proteins and their role during vertebrate’s development. Comp Biochem Physiol A Mol Integr Physiol 159:349–366

    PubMed  Google Scholar 

  • Sage TL, Bagha S, Lundsgaard-Nielsen V, Branch HA, Sultmanis S, Sage RF (2015) The effect of high temperature stress on male and female reproduction in plants. Field Crops Res 182:30–42

    Google Scholar 

  • Song X, Yuan L, Sundaresan V (2014) Antipodal cells persist through fertilization in the female gametophyte of Arabidopsis. Plant Reprod 27:197–203

    PubMed  Google Scholar 

  • Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c 1 [w]. Plant Physiol 139:1313–1322

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tayade R, Nguyen TD, Oh SA, Hwang YS, Yoon IS, Deshmuk R, Jung KH, Park SK (2018) Effective strategies for enhancing tolerance to high-temperature stress in rice during the reproductive and ripening stages. Plant Breed Biotechnol 6:1–18

    Google Scholar 

  • Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43:153–163

    CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    CAS  PubMed  Google Scholar 

  • Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenführer J, von Mering C, Grossniklaus U (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20:506–512

    CAS  PubMed  Google Scholar 

  • Xue H, Zhang F, Zhang ZH, Fu JF, Wang F, Zhang B, Ma Y (2015) Differences in salt tolerance between diploid and autotetraploid apple seedlings exposed to salt stress. Sci Hortic 190:24–30

    CAS  Google Scholar 

  • Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell. https://doi.org/10.1105/tpc.018192

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang SS, Yang H, Ding L, Song ZT, Ma H, Chang F, Liu JX (2017) Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in arabidopsis. Plant Cell 29:1007–1023

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Li Y, Liu H, Zhai X, Deng M, Dong Y, Fan G (2017a) Genome-wide expression analysis of salt-stressed diploid and autotetraploid Paulownia tomentosa. PLoS ONE 12(10):e0185455

    PubMed  PubMed Central  Google Scholar 

  • Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P et al (2017b) Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci USA 114:9326–9331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Prof. Venkatesan Sundaresan for the gift of CDC123::YFP seeds and Dr. Michal (Pellach) Leshem for critical reading of the manuscript. This work was supported by the Israel Science Foundation (ISF-UGC Research Grant No. 2713/16).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yehoram Leshem.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by Prem Bhalla.

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ambastha, V., Leshem, Y. Differential cell persistence is observed in the Arabidopsis female gametophyte during heat stress. Plant Reprod 33, 111–116 (2020). https://doi.org/10.1007/s00497-020-00390-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-020-00390-0

Keywords

Navigation