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Heat shock responses in Populus euphratica cell cultures: important role of crosstalk among hydrogen peroxide, calcium and potassium

Original Article

Abstract

Populus euphratica is an important woody species in north-west China that can survive extremely high temperatures. In the present study, the defensive responses of P. euphratica cells to moderate heat shock (HS, 48 °C) were investigated using fluorescence imaging technique and a non-invasive vibrating ion-selective microelectrode. HS induced a hydrogen peroxide (H2O2)—and caspase-like protease activity-dependent programmed cell death (PCD, <25 %) in P. euphratica cells. After HS, the total activities of antioxidant enzymes, such as catalase, ascorbate peroxidase and glutathione reductase, as well as those of non-enzymatic antioxidants, were significantly enhanced, leading to a decline in H2O2 accumulation. However, the upregulated antioxidant system was dependent on the activation of plasma membrane (PM) Ca2+-ATPase in HS-treated P. euphratica cells. In addition, H2O2, which was inhibited by the DPI (an inhibitor of PM NADPH oxidase as well as mitochondrial flavin-containing enzymes), was required for the activation of PM Ca2+-ATPase under HS condition. Moreover, HS induced an early influx of Ca2+ and an early efflux of K+ in P. euphratica cells. However, the inhibition of this Ca2+ influx and K+ efflux by GdCl3 and Tetraethylammonium chloride significantly decreased the production of H2O2. These results suggest that P. euphratica cells adapt to heat stress via the improvement of the antioxidant system. The upregulation of the antioxidant system is regulated by PM Ca2+-ATPase, H2O2, and the early activation of Ca2+ and K+ channels in the PM. Finally, a model was postulated to reveal the HS responses in P. euphratica cells.

Keywords

Heat shock responses Ca2+ K+ H2O2 PM Ca2+-ATPase Antioxidant system 

Abbreviations

HS

Heat shock

HSR

Heat shock response

HSPs

Heat shock proteins

HSFs

Heat stress transcription factors

H2O2

Hydrogen peroxide

PCD

Programmed cell death

CAT

Catalase

APX

Ascorbate peroxidase

GR

Glutathione reductase

TEA

Tetraethylammonium chloride

[Ca2+]cyt

Cytosolic free Ca2+

[Ca2+]vac

Vacuolar free Ca2+

H2DCF-DA

Dichlorodihydrofluorescein diacetate

DPI

Diphenyleneiodonium

DiBAC4(3)

Bis-(1,3-dibutylbarbituric acid)trimethine oxonol

NMT

Non-invasive micro-test technique

AsA

Reduced ascorbic acid

DHA

Dehydroascorbic acid

GSH

Reduced glutathione

GSSG

Oxidized glutathione

Eosin Y

Eosin yellow

MP

Membrane potential

Notes

Acknowledgments

This research was supported jointly by the National Science Foundation of China (Grant Nos. 31200470, 31270654), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), the Qing Lan Project, the Scientific Research Projects of Xuzhou City (No. XF13C056), the Research Project of Chinese Ministry of Education (Grant No. 113013A), the Key Project for Overseas Scholars by the Ministry of Human Resources and Social Security of PR China (Grant No. 2012001) and the Program of Introducing Talents of Discipline to Universities (111 Project, Grant No. B13007). The authors declare no conflict of interest.

Supplementary material

11240_2016_940_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 31 kb)

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Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institute of Integrative Plant Biology, School of Life ScienceJiangsu Normal UniversityXuzhouPeople’s Republic of China
  2. 2.College of Biological Sciences and TechnologyBeijing Forestry UniversityBeijingPeople’s Republic of China

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