The ER luminal binding protein (BiP) alleviates Cd2+-induced programmed cell death through endoplasmic reticulum stress–cell death signaling pathway in tobacco cells

Xu, Hua; Xu, Wenzhong; Xi, Hongmei; Ma, Wenwen; He, Zhenyan; Ma, Ming

doi:10.1016/j.jplph.2013.05.017

Cited by 60 publications

(52 citation statements)

References 52 publications

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“…BiP is an important molecular chaperone that confers plant stress resistance (Valente et al, 2009; Xu et al, 2013; Carvalho et al, 2014). In our study, the typical interim response genes BiP1 and BiP2 exhibited similar trends under both PEG stress and TUDCA pre-treatment.…”

Section: Resultsmentioning

confidence: 99%

“…In higher plants, studies have shown that this compound alleviates ER stress and cell death in Arabidopsis thaliana caused by the ER stress–inducers tunicamycin and dithiothreitol (Watanabe and Lam, 2008; Sun et al, 2013). Additional studies have also shown that TUDCA acts to inhibit heat- and Cd 2+ -induced ER stresses as well as cell apoptosis and augments heavy metal and heat stress tolerance in plants (Williams et al, 2010; Xu et al, 2013; Yang et al, 2014). …”

Section: Introductionmentioning

confidence: 99%

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Osmotic Stress Induced Cell Death in Wheat Is Alleviated by Tauroursodeoxycholic Acid and Involves Endoplasmic Reticulum Stress–Related Gene Expression

et al. 2017

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Although, tauroursodeoxycholic acid (TUDCA) has been widely studied in mammalian cells because of its role in inhibiting apoptosis, its effects on plants remain almost unknown, especially in the case of crops such as wheat. In this study, we conducted a series of experiments to explore the effects and mechanisms of action of TUDCA on wheat growth and cell death induced by osmotic stress. Our results show that TUDCA: (1) ameliorates the impact of osmotic stress on wheat height, fresh weight, and water content; (2) alleviates the decrease in chlorophyll content as well as membrane damage caused by osmotic stress; (3) decreases the accumulation of reactive oxygen species (ROS) by increasing the activity of antioxidant enzymes under osmotic stress; and (4) to some extent alleviates osmotic stress–induced cell death probably by regulating endoplasmic reticulum (ER) stress–related gene expression, for example expression of the basic leucine zipper genes bZIP60B and bZIP60D, the binding proteins BiP1 and BiP2, the protein disulfide isomerase PDIL8-1, and the glucose-regulated protein GRP94. We also propose a model that illustrates how TUDCA alleviates osmotic stress–related wheat cell death, which provides an important theoretical basis for improving plant stress adaptation and elucidates the mechanisms of ER stress–related plant osmotic stress resistance.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Osmotic Stress Induced Cell Death in Wheat Is Alleviated by Tauroursodeoxycholic Acid and Involves Endoplasmic Reticulum Stress–Related Gene Expression

et al. 2017

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“…ORF3+ is believed to help protein folding in ER to resolve ER stress like OsBIP1-OsBIP5 in the HSP70 gene family (Yang et al, 2012;Hayashi et al, 2013;Wakasa et al, 2014). BIP protein alleviates Cd 2+ stress-induced PCD (Xu et al, 2013). The tobacco (Nicotiana tabacum) plants with overexpression of BIP show delayed leaf senescence (Carvalho et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Processes Underlying a Reproductive Barrier in indica-japonica Rice Hybrids Revealed by Transcriptome Analysis

Zhu

Cheng

et al. 2017

Plant Physiol.

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In rice (Oryza sativa), hybrids between indica and japonica subspecies are usually highly sterile, which provides a model system for studying postzygotic reproductive isolation. A killer-protector system, S5, composed of three adjacent genes (ORF3, ORF4, and ORF5), regulates female gamete fertility of indica-japonica hybrids. To characterize the processes underlying this system, we performed transcriptomic analyses of pistils from rice variety Balilla (BL), Balilla with transformed ORF5+ (BL5+) producing sterile female gametes, and Balilla with transformed ORF3+ and ORF5+ (BL3+5+) producing fertile gametes. RNA sequencing of tissues collected before (MMC), during (MEI), and after (AME) meiosis of the megaspore mother cell detected 19,269 to 20,928 genes as expressed. Comparison between BL5+ and BL showed that ORF5+ induced differential expression of 8,339, 6,278, and 530 genes at MMC, MEI, and AME, respectively. At MMC, large-scale differential expression of cell wall-modifying genes and biotic and abiotic response genes indicated that cell wall integrity damage induced severe biotic and abiotic stresses. The processes continued to MEI and induced endoplasmic reticulum (ER) stress as indicated by differential expression of ER stress-responsive genes, leading to programmed cell death at MEI and AME, resulting in abortive female gametes. In the BL3 +5+/BL comparison, 3,986, 749, and 370 genes were differentially expressed at MMC, MEI, and AME, respectively. Large numbers of cell wall modification and biotic and abiotic response genes were also induced at MMC but largely suppressed at MEI without inducing ER stress and programed cell death , producing fertile gametes. These results have general implications for the understanding of biological processes underlying reproductive barriers.Reproductive isolation, a phenomenon widely existing in natural organisms, promotes speciation and maintains the integrity of species over time (Coyne and Orr, 2004). It is divided into two general categories depending on whether it occurs before or after fertilization: prezygotic reproductive isolation and postzygotic reproductive isolation (Seehausen et al., 2014). The former prevents the formation of hybrid zygotes, while the latter results in hybrid incompatibility, including hybrid necrosis, weakness, sterility, and lethality in F 1 or later generations (Ouyang and Zhang, 2013). The Dobzhansky-Muller model suggests that hybrid incompatibility is caused by the negative interactions between functionally divergent genes in the parental species (Dobzhansky, 1937;Muller, 1942).Rice (Oryza sativa), a major food crop and model plant for genomic study of monocotyledon species, also provides a model system for studying reproductive isolation. The Asian cultivated rice is composed of two subspecies, indica and japonica. Their hybrids are usually highly sterile, which is a barrier for utilization of the strong vigor in indica-japonica hybrids. A number of loci responsible for hybrid sterility have been identified, including ones that cause ...

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“…Many reports of heavy metal-induced PCD focused on Cd toxicity (Liu et al 2008;Xu et al 2013;Ye et al 2013). Huang et al (2014) reported that Al stress triggers mitochondria-dependent programmed cell death in peanut root tip cells.…”

Section: Discussionmentioning

confidence: 99%

Early generation of nitric oxide contributes to copper tolerance through reducing oxidative stress and cell death in hulless barley roots

2016

J Plant Res

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The objective of this study was to investigate the specific role of nitric oxide (NO) in the early response of hulless barley roots to copper (Cu) stress. We used the fluorescent probe diaminofluorescein-FM diacetate to establish NO localization, and hydrogen peroxide (H2O2)-special labeling and histochemical procedures for the detection of reactive oxygen species (ROS) in the root apex. An early production of NO was observed in Cu-treated root tips of hulless barley, but the detection of NO levels was decreased by supplementation with a NO scavenger, 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (c-PTIO). Application of sodium nitroprusside (a NO donor) relieved Cu-induced root inhibition, ROS accumulation and oxidative damage, while c-PTIO treatment had a synergistic effect with Cu and further enhanced ROS levels and oxidative stress. In addition, the Cu-dependent increase in activities of superoxide dismutase, peroxidase and ascorbate peroxidase were further enhanced by exogenous NO, but application of c-PTIO decreased the activities of catalase and ascorbate peroxidase in Cu-treated roots. Subsequently, cell death was observed in root tips and was identified as a type of programed cell death (PCD) by terminal deoxynucleotidyl transferase dUTP nick end labeling assay. The addition of NO prevented the increase of cell death in root tips, whereas inhibiting NO accumulation further increased the number of cells undergoing PCD. These results revealed that NO production is an early response of hulless barley roots to Cu stress and that NO contributes to Cu tolerance in hulless barley possibly by modulating antioxidant defense, subsequently reducing oxidative stress and PCD in root tips.

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The ER luminal binding protein (BiP) alleviates Cd2+-induced programmed cell death through endoplasmic reticulum stress–cell death signaling pathway in tobacco cells

Cited by 60 publications

References 52 publications

Osmotic Stress Induced Cell Death in Wheat Is Alleviated by Tauroursodeoxycholic Acid and Involves Endoplasmic Reticulum Stress–Related Gene Expression

Osmotic Stress Induced Cell Death in Wheat Is Alleviated by Tauroursodeoxycholic Acid and Involves Endoplasmic Reticulum Stress–Related Gene Expression

Processes Underlying a Reproductive Barrier in indica-japonica Rice Hybrids Revealed by Transcriptome Analysis

Early generation of nitric oxide contributes to copper tolerance through reducing oxidative stress and cell death in hulless barley roots

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