Heat Shock Protein 101 Plays a Crucial Role in Thermotolerance in Arabidopsis

Abstract

Plants are sessile organisms, and their ability to adapt to stress is crucial for survival in natural environments. Many observations suggest a relationship between stress tolerance and heat shock proteins (HSPs) in plants, but the roles of individual HSPs are poorly characterized. We report that transgenic Arabidopsis plants expressing less than usual amounts of HSP101, a result of either antisense inhibition or cosuppression, grew at normal rates but had a severely diminished capacity to acquire heat tolerance after mild conditioning pretreatments. The naturally high tolerance of germinating seeds, which express HSP101 as a result of developmental regulation, was also profoundly decreased. Conversely, plants constitutively expressing HSP101 tolerated sudden shifts to extreme temperatures better than did vector controls. We conclude that HSP101 plays a pivotal role in heat tolerance in Arabidopsis. Given the high evolutionary conservation of this protein and the fact that altering HSP101 expression had no detrimental effects on normal growth or development, one should be able to manipulate the stress tolerance of other plants by altering the expression of this protein. INTRODUCTIONOrganisms have evolved a wide array of mechanisms for adapting to stressful environments. One of the most closely studied of these is the induction of heat shock proteins (HSPs), which comprise several evolutionarily conserved protein families. All of the major HSPs (that is, those expressed in very high amounts in response to heat and other stresses) have related functions: they ameliorate problems caused by protein misfolding and aggregation. However, each major HSP family has a unique mechanism of action. Some promote the degradation of misfolded proteins (Lon, ubiquitin, and various ubiquitin-conjugating enzymes); others bind to different types of folding intermediates and prevent them from aggregating (Hsp70 and Hsp60); and still another (Hsp100) promotes the reactivation of proteins that have already aggregated Lindquist, 1993, 1994).Although all organisms synthesize HSPs in response to heat, the balance of proteins synthesized and the relative importance of individual HSP families in stress tolerance vary greatly among organisms. For example, in yeast , a member of the Hsp100 (ClpB/C) family, Hsp104, is strongly expressed in the nuclear-cytoplasmic compartment in response to stress and plays a particularly pivotal role in tolerance to extreme conditions (Sanchez et al., 1992;. Yeast cells expressing Hsp104 survive exposure to high temperatures or high concentrations of ethanol 1000-to 10,000-fold better than do cells not expressing Hsp104. Members of the Hsp100 family also play critical roles in the stress tolerance of bacterial cells (Schirmer et al., 1996), including photosynthetic cyanobacteria (Eriksson and Clarke, 1996). In contrast, the fruit fly Drosophila makes no protein of this type in response to stress; instead, the induction of Hsp70 plays the central role in stress tolerance in this organism (Solomon et al., 19...

Effects of high light on transcripts of stress-associated genes for the cyanobacteria Synechocystis sp. PCC 6803 and Prochlorococcus MED4 and MIT9313

“…PCC 6803. This agrees with the observation that in most eukaryotes, Hsp70s (the DnaK homologues) are represented by a multigene family in which the different family members are differentially expressed (Lindquist & Craig, 1988;Queitsch et al, 2000).…”

empty pericarp2 Encodes a Negative Regulator of the Heat Shock Response and Is Required for Maize Embryogenesis

“…In addition, transcripts of maize hsp101 also were upregulated in emp2 kernels at 16 DAP. Unlike hsp70 and dnaj, which are upregulated at the onset of heat shock, hsp101 was upregulated only after extended thermal stress (Queitsch et al, 2000). Thus, the overaccumulation of hsp101 transcripts indicates that emp2 mutant kernels are unable to attenuate the HSR.…”

Genetic approaches towards overcoming water deficit in plants - special emphasis on LEAs

“…Certain members of plant SHSPs are concerned with stabilization or reactivation of inactivated enzymes and overexpression studies have conferred stress tolerance in the transgenics. Expression of HSP101 (Queitsch et al, 2000;Katiyar-Agarwal et al, 2003), HSP17.6A (Sun et al, 2001) and antisense expression of HSP70 (Lee and Schoffl, 1996) in plants has been accomplished resulting in enhanced thermotolerance. Overexpression of DNAK1, an HSP70 member from the halotolerant Cyanobacterium aphanothece, in the cytosol of transgenic tobacco plants bestowed salt tolerance (Sugino et al, 1999).…”