The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption

PLoS One. 2014 Jan 29;9(1):e86661. doi: 10.1371/journal.pone.0086661. eCollection 2014.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological
  • Desiccation
  • Droughts
  • Endoplasmic Reticulum Chaperone BiP
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant*
  • Glycine max / genetics*
  • Glycine max / metabolism
  • Heat-Shock Proteins / genetics*
  • Heat-Shock Proteins / metabolism
  • Homeostasis / genetics*
  • Molecular Sequence Annotation
  • Plant Leaves / genetics*
  • Plant Leaves / metabolism
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Stress, Physiological / genetics
  • Transcriptome

Substances

  • Endoplasmic Reticulum Chaperone BiP
  • Heat-Shock Proteins
  • Plant Proteins

Grants and funding

This research was funded through the following grants from Brazilian Government Agencies: CNPq grants 573600/2008-2 and 470287/2011-0 (to EPBF); FAPEMIG grant CBB-APQ-00070-09; and FINEP grant 01.09.0625.00 (to EPBF). GCM and PAAR were supported by CNPq graduate fellowships, and HHC was supported by a FAPEMIG graduate fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.