The Molecular Chaperone Binding Protein BiP Prevents Leaf Dehydration-Induced Cellular Homeostasis Disruption

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.

Species‐specific spring and autumn leaf phenology captured by time‐lapse digital cameras

“…The diverse responses among eight species to drought in autumn (Table ) could be related to species‐specific physiological response mechanisms to environmental stresses, and the molecular and physiological responses to drought stress by gene regulation on plant hormones and stress‐shock proteins (Carvalho et al. ). Species that are less drought tolerant (e.g., white ash, maples, and black birch; Pääkkönen et al.…”

Deciduous forest responses to temperature, precipitation, and drought imply complex climate change impacts

“…We found that moderate summer heat-stress, summer and fall drought-stress, and summer heavy rain events, all lead to later autumn dormancy, counter to the traditional expectations. Studies on economically important plants (e.g., apples, soybeans, birch) have shown that under moderate heat-or water-stress in summer and fall, associated changes occur in gene-regulated levels of plant hormones and stress-shock proteins (44)(45)(46). The regulatory and physiological changes not only induce greater drought tolerance in plant leaves (47), but also prevent drought-induced cell death in leaves (that would otherwise lead to leaf senescence), and alter photosynthate source-sink relationships among plant organs (roots, stems, and leaves).…”

“…However, this phenomenon has been little studied (45). Few studies have mentioned either the effects of heat-and drought-stress on fall phenology (45,48) or the potential role of the underlying molecular and physiological mechanisms (44,46). We have an ongoing project of groundbased phenological observations (SI Appendix, Fig.…”

Genome-wide identification and characterization ofSolanum tuberosum BiPgenes reveals the role of the promoter architecture in BiP gene diversity

“…All BiP proteins have C-terminal HDEL or KDEL signaling motif, which ensures their retention and function in the ER and an ATP-binding domain near the N-terminus 2 .Across eukaryotes, BiPs are among the most abundant chaperones in the ER and are directly engaged in regulating the unfolded protein response (UPR). Under normal conditions in mammalian cells, BiP binds to and inhibits the three ER stress sensors, protein kinase RNA-like ER kinase (PERK), activating transcription factor 6 (ATF6), and inositol-requiring enzyme 1α (IRE1α) 3,4 . BiP releases the sensors to activate ER-to-nucleus signaling cascades.…”

“…protein (NRP) and vacuolar processing enzyme [1][2][3][4] . The Arabidopsis, pepper, rice, soybean, and wheat genomes encode three or four BiPs which have been annotated and, extensive studies have revealed that many of these plant BiP proteins play crucial roles in biotic stress resistance and plant innate immunity [5][6][7][8][9] .…”