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...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2014-01-01
|
| Series: | PLoS ONE |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24489761/?tool=EBI |
| _version_ | 1818338041318604800 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-13T15:04:48Z |
| format | Article |
| id | doaj.art-60540b2c35454a5b9178fdc607e2c000 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-13T15:04:48Z |
| publishDate | 2014-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-60540b2c35454a5b9178fdc607e2c0002022-12-21T23:41:02ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0191e8666110.1371/journal.pone.0086661The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption.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 FontesBiP 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.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24489761/?tool=EBI |
| spellingShingle | 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. PLoS ONE |
| title | 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_short | 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 |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24489761/?tool=EBI |
| work_keys_str_mv | AT humbertohcarvalho themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT otaviojbbrustolini themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT maianarpimenta themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT gisellecmendes themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT biancacgouveia themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT priscilaasilva themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT josecleydsonfsilva themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT clenilsosmota themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT julianarlsoaresramos themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT elizabethpbfontes themolecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT humbertohcarvalho molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT otaviojbbrustolini molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT maianarpimenta molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT gisellecmendes molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT biancacgouveia molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT priscilaasilva molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT josecleydsonfsilva molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT clenilsosmota molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT julianarlsoaresramos molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption AT elizabethpbfontes molecularchaperonebindingproteinbippreventsleafdehydrationinducedcellularhomeostasisdisruption |