The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption.
BiP overexpression improves leaf water relations during droughts and delays drought-induced leaf senescence. However, whether BiP controls cellular homeostasis under drought conditions or simply delays dehydration-induced leaf senescence as the primary cause for water stress tolerance remains to be...
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oai:doaj.org-article:60540b2c35454a5b9178fdc607e2c0002021-11-18T08:35:09ZThe molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption.1932-620310.1371/journal.pone.0086661https://doaj.org/article/60540b2c35454a5b9178fdc607e2c0002014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24489761/?tool=EBIhttps://doaj.org/toc/1932-6203BiP overexpression improves leaf water relations during droughts and delays drought-induced leaf senescence. However, whether BiP controls cellular homeostasis under drought conditions or simply delays dehydration-induced leaf senescence as the primary cause for water stress tolerance remains to be determined. To address this issue, we examined the drought-induced transcriptomes of BiP-overexpressing lines and wild-type (WT) lines under similar leaf water potential (ψw) values. In the WT leaves, a ψw reduction of -1.0 resulted in 1339 up-regulated and 2710 down-regulated genes; in the BiP-overexpressing line 35S::BiP-4, only 334 and 420 genes were induced and repressed, respectively, at a similar leaf ψw = -1.0 MPa. This level of leaf dehydration was low enough to induce a repertory of typical drought-responsive genes in WT leaves but not in 35S::BiP-4 dehydrated leaves. The responders included hormone-related genes, functional and regulatory genes involved in drought protection and senescence-associated genes. The number of differentially expressed genes in the 35S::BiP-4 line approached the wild type number at a leaf ψw = -1.6 MPa. However, N-rich protein (NRP)- mediated cell death signaling genes and unfolded protein response (UPR) genes were induced to a much lower extent in the 35S::BiP-4 line than in the WT even at ψw = -1.6 MPa. The heatmaps for UPR, ERAD (ER-associated degradation protein system), drought-responsive and cell death-associated genes revealed that the leaf transcriptome of 35S::BiP-4 at ψw = -1.0 MPa clustered together with the transcriptome of well-watered leaves and they diverged considerably from the drought-induced transcriptome of the WT (ψw = -1.0, -1.7 and -2.0 MPa) and 35S::BiP-4 leaves at ψw = -1.6 MPa. Taken together, our data revealed that BiP-overexpressing lines requires a much higher level of stress (ψw = -1.6 MPa) to respond to drought than that of WT (ψw = -1.0). Therefore, BiP overexpression maintains cellular homeostasis under water stress conditions and thus ameliorates endogenous osmotic stress.Humberto H CarvalhoOtávio J B BrustoliniMaiana R PimentaGiselle C MendesBianca C GouveiaPriscila A SilvaJosé Cleydson F SilvaClenilso S MotaJuliana R L Soares-RamosElizabeth P B FontesPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 9, Iss 1, p e86661 (2014) |
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Medicine R Science Q |
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Medicine R Science Q Humberto H Carvalho Otávio J B Brustolini Maiana R Pimenta Giselle C Mendes Bianca C Gouveia Priscila A Silva José Cleydson F Silva Clenilso S Mota Juliana R L Soares-Ramos Elizabeth P B Fontes The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. |
| description |
BiP overexpression improves leaf water relations during droughts and delays drought-induced leaf senescence. However, whether BiP controls cellular homeostasis under drought conditions or simply delays dehydration-induced leaf senescence as the primary cause for water stress tolerance remains to be determined. To address this issue, we examined the drought-induced transcriptomes of BiP-overexpressing lines and wild-type (WT) lines under similar leaf water potential (ψw) values. In the WT leaves, a ψw reduction of -1.0 resulted in 1339 up-regulated and 2710 down-regulated genes; in the BiP-overexpressing line 35S::BiP-4, only 334 and 420 genes were induced and repressed, respectively, at a similar leaf ψw = -1.0 MPa. This level of leaf dehydration was low enough to induce a repertory of typical drought-responsive genes in WT leaves but not in 35S::BiP-4 dehydrated leaves. The responders included hormone-related genes, functional and regulatory genes involved in drought protection and senescence-associated genes. The number of differentially expressed genes in the 35S::BiP-4 line approached the wild type number at a leaf ψw = -1.6 MPa. However, N-rich protein (NRP)- mediated cell death signaling genes and unfolded protein response (UPR) genes were induced to a much lower extent in the 35S::BiP-4 line than in the WT even at ψw = -1.6 MPa. The heatmaps for UPR, ERAD (ER-associated degradation protein system), drought-responsive and cell death-associated genes revealed that the leaf transcriptome of 35S::BiP-4 at ψw = -1.0 MPa clustered together with the transcriptome of well-watered leaves and they diverged considerably from the drought-induced transcriptome of the WT (ψw = -1.0, -1.7 and -2.0 MPa) and 35S::BiP-4 leaves at ψw = -1.6 MPa. Taken together, our data revealed that BiP-overexpressing lines requires a much higher level of stress (ψw = -1.6 MPa) to respond to drought than that of WT (ψw = -1.0). Therefore, BiP overexpression maintains cellular homeostasis under water stress conditions and thus ameliorates endogenous osmotic stress. |
| format |
article |
| author |
Humberto H Carvalho Otávio J B Brustolini Maiana R Pimenta Giselle C Mendes Bianca C Gouveia Priscila A Silva José Cleydson F Silva Clenilso S Mota Juliana R L Soares-Ramos Elizabeth P B Fontes |
| author_facet |
Humberto H Carvalho Otávio J B Brustolini Maiana R Pimenta Giselle C Mendes Bianca C Gouveia Priscila A Silva José Cleydson F Silva Clenilso S Mota Juliana R L Soares-Ramos Elizabeth P B Fontes |
| author_sort |
Humberto H Carvalho |
| title |
The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. |
| title_short |
The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. |
| title_full |
The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. |
| title_fullStr |
The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. |
| title_full_unstemmed |
The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. |
| title_sort |
molecular chaperone binding protein bip prevents leaf dehydration-induced cellular homeostasis disruption. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2014 |
| url |
https://doaj.org/article/60540b2c35454a5b9178fdc607e2c000 |
| work_keys_str_mv |
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