The Transcriptional Co-activator MBF1c Is a Key Regulator of Thermotolerance in Arabidopsis thalianaNobuhiro Suzuki, Sunil Bajad, Joel L. Shuman et al.|Journal of Biological Chemistry|2008 The ability of an organism to acclimate to its environment is a key determinant in its global distribution and capacity to compete with other organisms. The heat stress response, a highly conserved environmental and developmental program in eukaryotic and prokaryotic organisms, is an important component of the acclimation response of plants. Previous studies have shown that heat shock transcription factors play an important role in thermotolerance in plants and other organisms, controlling the expression of different heat shock proteins and detoxifying enzymes. In contrast, although several other pathways, involving ethylene, salicylic acid (SA), and trehalose, were recently shown to play a central role in thermotolerance in plants, a key regulator of these responses was not identified. Here we report that the highly conserved transcriptional co-activator, MBF1c (multiprotein bridging factor 1c), is a key regulator of thermotolerance in Arabidopsis thaliana. MBF1c protein accumulates rapidly and is localized to nuclei during heat stress. MBF1c is required for thermotolerance and functions upstream to SA, trehalose, ethylene, and pathogenesis-related protein 1 during heat stress. In contrast, MBF1c is not required for the expression of transcripts encoding HSFA2 and different heat shock proteins. Interestingly, MBF1c interacts with TPS5 (trehalose phosphate synthase 5), which is also heat-inducible, and mutants deficient in TPS5 are thermosensitive. Our results provide evidence for the existence of a tightly coordinated heat stress-response network, involving trehalose-, SA-, and ethylene-signaling pathways, that is under the control of MBF1c. The ability of an organism to acclimate to its environment is a key determinant in its global distribution and capacity to compete with other organisms. The heat stress response, a highly conserved environmental and developmental program in eukaryotic and prokaryotic organisms, is an important component of the acclimation response of plants. Previous studies have shown that heat shock transcription factors play an important role in thermotolerance in plants and other organisms, controlling the expression of different heat shock proteins and detoxifying enzymes. In contrast, although several other pathways, involving ethylene, salicylic acid (SA), and trehalose, were recently shown to play a central role in thermotolerance in plants, a key regulator of these responses was not identified. Here we report that the highly conserved transcriptional co-activator, MBF1c (multiprotein bridging factor 1c), is a key regulator of thermotolerance in Arabidopsis thaliana. MBF1c protein accumulates rapidly and is localized to nuclei during heat stress. MBF1c is required for thermotolerance and functions upstream to SA, trehalose, ethylene, and pathogenesis-related protein 1 during heat stress. In contrast, MBF1c is not required for the expression of transcripts encoding HSFA2 and different heat shock proteins. Interestingly, MBF1c interacts with TPS5 (trehalose phosphate synthase 5), which is also heat-inducible, and mutants deficient in TPS5 are thermosensitive. Our results provide evidence for the existence of a tightly coordinated heat stress-response network, involving trehalose-, SA-, and ethylene-signaling pathways, that is under the control of MBF1c. Thermotolerance is an essential component of the acclimation response of different organisms (1Craig E.A. CRC Crit. Rev. Biochem. 1985; 18: 239-280Crossref Rev. Rev. is thermotolerance the ability to to heat and thermotolerance the ability to the Previous studies have shown that heat shock transcription factors shock transcription shock bridging factor phosphate shock transcription shock bridging factor phosphate play an important role in thermotolerance in plants and other organisms, heat shock proteins different acclimation and proteins In contrast, although several other pathways, involving ethylene, salicylic acid (SA), and trehalose, have recently to play an important role in thermotolerance in plants a key regulator of these responses was not (multiprotein bridging factor is a highly conserved transcriptional in the of central and 18: proteins different organisms with transcription and with different and with the protein 18: The Arabidopsis different encoding of which in and are In contrast, the expression of MBF1c is in Arabidopsis in response to and of the acid we report that MBF1c is a key regulator of thermotolerance in MBF1c is required for thermotolerance and functions upstream to SA, trehalose, and during heat stress. In contrast, MBF1c is not required for thermotolerance the expression of HSFA2 and different Interestingly, MBF1c with a protein to in (trehalose phosphate synthase and is localized to the nuclei of during heat and plants were under mutants for MBF1c and TPS5 and were and in in under and not and were in to the of MBF1c was in plants under the control of the a and a an with control for nuclei was to a and mutants were for heat stress studies of and mutants were for heat stress studies of TPS5 and thermotolerance were in and The of acid were in and a the of and plants were to and and plants were in were in and was in and and protein were and to to the were for was to the for was in and was the of in for and was in of the was The for was and of MBF1c was in the MBF1c expression was 1 in 1 of for were and MBF1c was in 1 and MBF1c protein was and for the of of MBF1c in protein rapidly in Arabidopsis during heat stress In contrast, MBF1c protein was not in plants under in a of MBF1c MBF1c protein was in plants MBF1c under to heat stress The of MBF1c protein protein in Arabidopsis plants to the of the MBF1c not of protein and control protein were in plants under the control of the and plants with expression of were under protein was localized to the In contrast, plants were to heat stress protein was in the of the control protein was not response, with different was not an of that of MBF1c during heat stress is a of of in MBF1c of MBF1c was and to heat stress. not MBF1c protein in response to heat stress and were to heat stress for to thermotolerance for to for 1 and to for to plants were not deficient in thermotolerance were deficient in thermotolerance different In to plants, plants were to thermotolerance was also the was for plants The thermotolerance of the MBF1c a of MBF1c expression and shown in MBF1c protein in to heat stress for and to thermotolerance of and MBF1c plants. of and to heat stress for to thermotolerance for to for 1 and to for to were also plants of with expression of MBF1c 1 and plants with the MBF1c expression in plants with MBF1c 1 and were in was to the not The expression of MBF1c in the different is with that of MBF1c in the plants in and in protein expression of MBF1c in to heat stress for and to in MBF1c during expression of MBF1c was heat stress In contrast, MBF1c was not in plants. with expression of several different and was not in plants during heat stress In contrast, protein expression was not in plants during heat and the expression of transcripts encoding the response protein was in plants with plants during heat stress. In to and with plants, the expression of which functions a in plants during heat stress The expression of MBF1c during heat was not in mutants deficient in and of transcripts encoding different and acclimation proteins in MBF1c plants during heat stress. were and plants different heat stress was to control for of MBF1c with was for the of MBF1c. we a Arabidopsis to different were for were and and and also an and proteins and that are were with TPS5 in in in expression of TPS5 was to in and plants during heat stress was and a in TPS5 expression during heat stress in plants In contrast, TPS5 expression was in plants in the of stress during heat stress Interestingly, the of TPS5 was in plants in the of heat stress In of transcripts in Arabidopsis that TPS5 is the during heat stress in Arabidopsis TPS5 mutants were deficient in not thermotolerance of MBF1c with of MBF1c and TPS5 of MBF1c and TPS5 were and and a was 1 TPS5 expression in and plants during heat stress and were TPS5 expression in and plants during heat stress expression of and transcripts in Arabidopsis during heat stress. were the thermotolerance of and of MBF1c in during in plants during heat stress and in plants under and In contrast, not during heat stress in plants that MBF1c functions upstream to during heat stress. plants heat stress. was to plants and and mutants deficient in and and plants were deficient in studies MBF1c and In to the results with plants, not the heat of plants that MBF1c that the of thermotolerance in and and plants is in plants. is also the that the thermotolerance of plants and to the in plants and that plants and in and plants. of in and plants different during heat stress of in and plants different during heat stress of and in and plants under of during heat stress trehalose, SA, and of and and during heat stress of and and during heat stress of and and during heat stress of plants during heat stress were to heat stress in the of trehalose, SA, and for to during expression was in and plants that MBF1c is not required for in plants during heat stress and in plants under and In contrast, not in plants during heat stress that MBF1c is required for during heat stress in was to plants a deficient in and and and plants a of in that MBF1c functions upstream to during heat stress. In to the of the thermotolerance of to the heat stress that functions to of in the thermotolerance of not the of plants that MBF1c to heat stress and these plants were to under to during an and a deficient in heat stress In contrast, plants expression not in plants during heat stress In contrast, expression was in plants during heat stress. Our results a in which MBF1c functions upstream to that functions upstream to and during heat stress. The expression of during heat stress not to expression is in and plants during heat stress and In contrast, expression was not in plants that expression is of TPS5 and that SA, ethylene, and TPS5 during heat stress In to expression of HSFA2 was in mutants during heat stress that plants are to for the heat shock response for the role of MBF1c during heat stress in expression in and during heat stress 1 and expression in and during heat stress a for MBF1c MBF1c is to upstream to SA, ethylene, and during heat stress. In contrast, MBF1c is not to required for the expression of and during heat the role of MBF1c in thermotolerance in Arabidopsis is shown in Our a in which MBF1c functions upstream to trehalose, SA, and results a in which and of is not is a MBF1c trehalose, is to proteins are highly conserved in different organisms, and plants 18: Our an that proteins other organisms are also in responses to stress. The in MBF1c and during heat stress and also in other organisms, is to play a key and role during different environmental stress in plants, is that functions a Previous studies have key of to a transcripts encoding TPS5 were to during heat and mutants of TPS5 were deficient in thermotolerance to a of in the of different in Arabidopsis and that have in during different environmental of evidence the that MBF1c and TPS5 The expression of TPS5 and MBF1c is during heat stress TPS5 and MBF1c were to in and in and mutants for TPS5 and MBF1c are to not thermotolerance and MBF1c expression of TPS5 and not during heat stress and plants transcripts encoding TPS5 and and and plants heat stress studies are required to the that MBF1c its with is to a transcriptional was shown to in that in transcription of The of MBF1c protein to nuclei during stress and the of a conserved in MBF1c the that MBF1c functions in plants a transcriptional of plants, under and that a of the transcripts in plants were with ethylene, SA, and of plants and that MBF1c a transcriptional regulator that the expression of transcripts in plants in the of stress. is that the of MBF1c protein in the nuclei of plants, under ethylene, SA, and of and MBF1c plants evidence for a MBF1c and a role for MBF1c a central regulator of thermotolerance in and that MBF1c functions upstream to SA, ethylene, and during heat stress. the expression of MBF1c is in response to different is that the role of MBF1c in the response of plants to different is that in In of plants were to to heat to Thermotolerance is an essential component of the acclimation response of different organisms (1Craig E.A. CRC Crit. Rev. Biochem. 1985; 18: 239-280Crossref Rev. Rev. is thermotolerance the ability to to heat and thermotolerance the ability to the Previous studies have shown that heat shock transcription factors shock transcription shock bridging factor phosphate shock transcription shock bridging factor phosphate play an important role in thermotolerance in plants and other organisms, heat shock proteins different acclimation and proteins In contrast, although several other pathways, involving ethylene, salicylic acid (SA), and trehalose, have recently to play an important role in thermotolerance in plants a key regulator of these responses was not identified. heat shock transcription factor heat shock protein protein acid salicylic acid bridging factor 1 phosphate synthase heat shock transcription factor heat shock protein protein acid salicylic acid bridging factor 1 phosphate synthase (multiprotein bridging factor is a highly conserved transcriptional in the of central and 18: proteins different organisms with transcription and with different and with the protein 18: The Arabidopsis different encoding of which in and are In contrast, the expression of MBF1c is in Arabidopsis in response to and of the acid Here we report that MBF1c is a key regulator of thermotolerance in MBF1c is required for thermotolerance and functions upstream to SA, trehalose, and during heat stress. In contrast, MBF1c is not required for thermotolerance the expression of HSFA2 and different Interestingly, MBF1c with a protein to in (trehalose phosphate synthase and is localized to the nuclei of during heat stress. and plants were under mutants for MBF1c and TPS5 and were and in in under and not and were in to the of MBF1c was in plants under the control of the a and a an with control for nuclei was to a and mutants were for heat stress studies of and mutants were for heat stress studies of TPS5 and thermotolerance were in and The of acid were in and a the of and plants were to and and plants were in were in and was in and and protein were and to to the were for was to the for was in and was the of in for and was in of the was The for was and of MBF1c was in the MBF1c expression was 1 in 1 of for were and MBF1c was in 1 and MBF1c protein was and for the of and plants were under mutants for MBF1c and TPS5 and were and in in under and not and were in to the of MBF1c was in plants under the control of the a and a an with control for nuclei was to a and mutants were for heat stress studies of and mutants were for heat stress studies of TPS5 and thermotolerance were in and The of acid were in and a the of and plants were to and and plants were in were in and was in and and protein were and to to the were for was to the for was in and was the of in for and was in of the was The for was and of MBF1c was in the MBF1c expression was 1 in 1 of for were and MBF1c was in 1 and MBF1c protein was and for the of of MBF1c in protein rapidly in Arabidopsis during heat stress In contrast, MBF1c protein was not in plants under in a of MBF1c MBF1c protein was in plants MBF1c under to heat stress The of MBF1c protein protein in Arabidopsis plants to the of the MBF1c not of protein and control protein were in plants under the control of the and plants with expression of were under protein was localized to the In contrast, plants were to heat stress protein was in the of the control protein was not response, with different was not an of that of MBF1c during heat stress is a of of in MBF1c of MBF1c was and to heat stress. not MBF1c protein in response to heat stress and were to heat stress for to thermotolerance for to for 1 and to for to plants were not deficient in thermotolerance were deficient in thermotolerance different In to plants, plants were to thermotolerance was also the was for plants The thermotolerance of the MBF1c a of MBF1c expression and shown in MBF1c protein in to heat stress for and to thermotolerance in MBF1c during expression of MBF1c was heat stress In contrast, MBF1c was not in plants. with expression of several different and was not in plants during heat stress In contrast, protein expression was not in plants during heat and the expression of transcripts encoding the response protein was in plants with plants during heat stress. In to and with plants, the expression of which functions a in plants during heat stress The expression of MBF1c during heat was not in mutants deficient in and of transcripts encoding different and acclimation proteins in MBF1c plants during heat stress. were and plants different heat stress was to control for of MBF1c with was for the of MBF1c. we a Arabidopsis to different were for were and and and also an and proteins and that are were with TPS5 in in in expression of TPS5 was to in and plants during heat stress was and a in TPS5 expression during heat stress in plants In contrast, TPS5 expression was in plants in the of stress during heat stress Interestingly, the of TPS5 was in plants in the of heat stress In of transcripts in Arabidopsis that TPS5 is the during heat stress in Arabidopsis TPS5 mutants were deficient in not thermotolerance of MBF1c with of MBF1c and TPS5 of MBF1c and TPS5 were and and a was 1 TPS5 expression in and plants during heat stress and were TPS5 expression in and plants during heat stress expression of and transcripts in Arabidopsis during heat stress. were the thermotolerance of and of MBF1c in during in plants during heat stress and in plants under and In contrast, not during heat stress in plants that MBF1c functions upstream to during heat stress. plants heat stress. was to plants and and mutants deficient in and and plants were deficient in studies MBF1c and In to the results with plants, not the heat of plants that MBF1c that the of thermotolerance in and and plants is in plants. is also the that the thermotolerance of plants and to the in plants and that plants and in and plants. of in and plants different during heat stress of in and plants different during heat stress of and in and plants under of during heat stress trehalose, SA, and of and and during heat stress of and and during heat stress of and and during heat stress of plants during heat stress were to heat stress in the of trehalose, SA, and for to during expression was in and plants that MBF1c is not required for in plants during heat stress and in plants under and In contrast, not in plants during heat stress that MBF1c is required for during heat stress in was to plants a deficient in and and and plants a of in that MBF1c functions upstream to during heat stress. In to the of the thermotolerance of to the heat stress that functions to of in the thermotolerance of not the of plants that MBF1c to heat stress and these plants were to under to during an and a deficient in heat stress In contrast, plants expression not in plants during heat stress In contrast, expression was in plants during heat stress. Our results a in which MBF1c functions upstream to that functions upstream to and during heat stress. The expression of during heat stress not to expression is in and plants during heat stress and In contrast, expression was not in plants that expression is of TPS5 and that SA, ethylene, and TPS5 during heat stress In to expression of HSFA2 was in mutants during heat stress that plants are to for the heat shock response for the role of MBF1c during heat stress in expression in and during heat stress 1 and expression in and during heat stress a for MBF1c MBF1c is to upstream to SA, ethylene, and during heat stress. In contrast, MBF1c is not to required for the expression of and during heat of MBF1c in protein rapidly in Arabidopsis during heat stress In contrast, MBF1c protein was not in plants under in a of MBF1c MBF1c protein was in plants MBF1c under to heat stress The of MBF1c protein protein in Arabidopsis plants to the of the MBF1c not of protein and control protein were in plants under the control of the and plants with expression of were under protein was localized to the In contrast, plants were to heat stress protein was in the of the control protein was not response, with different was not an of that of MBF1c during heat stress is a of Thermotolerance of in MBF1c of MBF1c was and to heat stress. not MBF1c protein in response to heat stress and were to heat stress for to thermotolerance for to for 1 and to for to plants were not deficient in thermotolerance were deficient in thermotolerance different In to plants, plants were to thermotolerance was also the was for plants The thermotolerance of the MBF1c a of MBF1c expression and shown in MBF1c protein in to heat stress for and to thermotolerance in MBF1c during expression of MBF1c was heat stress In contrast, MBF1c was not in plants. with expression of several different and was not in plants during heat stress In contrast, protein expression was not in plants during heat and the expression of transcripts encoding the response protein was in plants with plants during heat stress. In to and with plants, the expression of which functions a in plants during heat stress The expression of MBF1c during heat was not in mutants deficient in and of MBF1c with was for the of MBF1c. we a Arabidopsis to different were for were and and and also an and proteins and that are were identified. MBF1c with TPS5 in in in expression of TPS5 was to in and plants during heat stress was and a in TPS5 expression during heat stress in plants In contrast, TPS5 expression was in plants in the of stress during heat stress Interestingly, the of TPS5 was in plants in the of heat stress In of transcripts in Arabidopsis that TPS5 is the during heat stress in Arabidopsis TPS5 mutants were deficient in not thermotolerance of MBF1c in during in plants during heat stress and in plants under and In contrast, not during heat stress in plants that MBF1c functions upstream to during heat stress. plants heat stress. was to plants and and mutants deficient in and and plants were deficient in studies MBF1c and In to the results with plants, not the heat of plants that MBF1c that the of thermotolerance in and and plants is in plants. is also the that the thermotolerance of plants and to the in plants and that plants MBF1c to during expression was in and plants that MBF1c is not required for in plants during heat stress and in plants under and In contrast, not in plants during heat stress that MBF1c is required for during heat stress in was to plants a deficient in and and and plants a of in that MBF1c functions upstream to during heat stress. In to the of the thermotolerance of to the heat stress that functions to of in the thermotolerance of not the of plants that MBF1c to heat stress and these plants were to under to during an and a deficient in heat stress In contrast, plants expression not in plants during heat stress In contrast, expression was in plants during heat stress. Our results a in which MBF1c functions upstream to that functions upstream to and during heat stress. The expression of during heat stress not to expression is in and plants during heat stress and In contrast, expression was not in plants that expression is of TPS5 and that SA, ethylene, and TPS5 during heat stress In to expression of HSFA2 was in mutants during heat stress that plants are to for the heat shock response the role of MBF1c in thermotolerance in Arabidopsis is shown in Our a in which MBF1c functions upstream to trehalose, SA, and results a in which and of is not is a MBF1c trehalose, is to proteins are highly conserved in different organisms, and plants 18: Our an that proteins other organisms are also in responses to stress. The in MBF1c and during heat stress and also in other organisms, is to play a key and role during different environmental stress in plants, is that functions a Previous studies have key of to a transcripts encoding TPS5 were to during heat and mutants of TPS5 were deficient in thermotolerance to a of in the of different in Arabidopsis and that have in during different environmental of evidence the that MBF1c and TPS5 The expression of TPS5 and MBF1c is during heat stress TPS5 and MBF1c were to in and in and mutants for TPS5 and MBF1c are to not thermotolerance and MBF1c expression of TPS5 and not during heat stress and plants transcripts encoding TPS5 and and and plants heat stress studies are required to the that MBF1c its with is to a transcriptional was shown to in that in transcription of The of MBF1c protein to nuclei during stress and the of a conserved in MBF1c the that MBF1c functions in plants a transcriptional of plants, under and that a of the transcripts in plants were with ethylene, SA, and of plants and that MBF1c a transcriptional regulator that the expression of transcripts in plants in the of stress. is that the of MBF1c protein in the nuclei of plants, under ethylene, SA, and of and MBF1c plants evidence for a MBF1c and a role for MBF1c a central regulator of thermotolerance in and that MBF1c functions upstream to SA, ethylene, and during heat stress. the expression of MBF1c is in response to different is that the role of MBF1c in the response of plants to different is that in In of plants were to to heat to the role of MBF1c in thermotolerance in Arabidopsis is shown in Our a in which MBF1c functions upstream to trehalose, SA, and results a in which and of is not is a MBF1c trehalose, is to proteins are highly conserved in different organisms, and plants 18: Our an that proteins other organisms are also in responses to stress. The in MBF1c and during heat stress and also in other organisms, is to play a key and role during different environmental stress in plants, is that functions a Previous studies have key of to a transcripts encoding TPS5 were to during heat and mutants of TPS5 were deficient in thermotolerance to a of in the of different in Arabidopsis and that have in during different environmental of evidence the that MBF1c and TPS5 The expression of TPS5 and MBF1c is during heat stress TPS5 and MBF1c were to in and in and mutants for TPS5 and MBF1c are to not thermotolerance and MBF1c expression of TPS5 and not during heat stress and plants transcripts encoding TPS5 and and and plants heat stress studies are required to the that MBF1c its with MBF1c is to a transcriptional was shown to in that in transcription of The of MBF1c protein to nuclei during stress and the of a conserved in MBF1c the that MBF1c functions in plants a transcriptional of plants, under and that a of the transcripts in plants were with ethylene, SA, and of plants and that MBF1c a transcriptional regulator that the expression of transcripts in plants in the of stress. is that the of MBF1c protein in the nuclei of plants, under ethylene, SA, and Our of and MBF1c plants evidence for a MBF1c and a role for MBF1c a central regulator of thermotolerance in and that MBF1c functions upstream to SA, ethylene, and during heat stress. the expression of MBF1c is in response to different is that the role of MBF1c in the response of plants to different is that in In of plants were to to heat to with with