Active BR signalling adjusts the subcellular localisation of BES1/HSP90 complex formation

Abstract

Heat shock proteins 90 (HSP90) are essential and play critical roles in the adaptation of organisms to diverse stimuli. In plants, HSP90 are involved in auxin, jasmonate and brassinosteroid (BR) signalling pathways. The BR‐promoted activation of the BES1 transcription factor regulates BR‐responsive genes. Using genetic, physiological, fluorescence live cell imaging, molecular and biochemical approaches, such as phenotypic analysis, co‐immunoprecipitation assay, yeast‐two hybrid and Bimolecular fluorescence complementation (BiFC), we studied complex formation between BES1 and HSP90 under control conditions and active BR signalling. Further, we determined the effect of the pharmacological inhibition of HSP90 ATPase activity on hypocotyl elongation of bes1-D mutant. We determined that HSP90 interact with BES1 in the nucleus and in the cytoplasm. During active BR signalling, nuclear complexes were absent while cytoplasmic HSP90/BES1 complexes were prominent. Our results showed that the hypocotyl length of bes1‐D mutants was highly reduced when HSP90 was challenged by the geldanamycin (GDA) inhibitor of the ATPase activity of HSP90. Active BR signalling could not rescue the GDA effect on the hypocotyl elongation of bes1-D. Our results reveal that the constitutively active BES1 in the bes1‐D mutant is hypersensitive to GDA. The interaction of HSP90 with BES1 argues that HSP90 facilitate the nuclear metastable conformation of BES1 to regulate BR‐dependent gene expression, and our data show that HSP90 assist in the compartmentalised cycle of BES1 during active BR signalling.

Linking Brassinosteroid and ABA Signaling in the Context of Stress Acclimation

“…Mutation in the HvBRI1 gene causes a decreased HSP level and decreased HSP gene expression [ 67 ]. Although it is known that HSPs interact with the BR core components [ 68 , 69 ], there is no evidence of such interaction with HSFs. If it is established that BR signaling components interact with HSFs, then studies of BRs in terms of the implementation of stress memory will receive a new direction, since HSFs are the main sculptors of the epigenetic landscape [ 70 ].…”

Phosphatidic acid and hydrogen peroxide coordinately enhance heat tolerance in tall fescue

“…2013; Samakovli et al . 2020). The HSP are downstream of HSF, and some HSP serve as molecular chaperones in plants, preventing protein aggregation and misfolding during heat stress (Kumar et al .…”

“…Heat shock factors are involved in stress signal perception and transduction and control the expression of heat stress proteins (HSP), which play key roles in intrinsic and acquired thermotolerance in plants (Hasanuzzaman et al 2013;Qu et al 2013;Samakovli et al 2020). The HSP are downstream of HSF, and some HSP serve as molecular chaperones in plants, preventing protein aggregation and misfolding during heat stress (Kumar et al 2015).…”

HSP90 affects root growth in Arabidopsis by regulating the polar distribution of PIN1

“…The interaction of HSP90 with kinases, transcription factors or brassinosteroid signaling components is dynamically affecting genetic circuitries leading to various developmental processes (Samakovli et al ., 2007, 2014; Lachowiec et al ., 2013; Shigeta et al ., 2015; Margaritopoulou et al ., 2016; Wang et al ., 2016; Watanabe et al ., 2016; Samakovli et al ., 2020a,b; Tichá et al ., 2020). In brassinosteroid signaling, HSP90 interacts and influences BIN2 and BES1 complex localization while HSP90 nuclear localization is influenced by brassinolide (BL; Samakovli et al ., 2014, 2020a). HSP90 interacts with YODA kinase influencing its polarization and regulating the phosphorylation of the downstream signaling kinase components, like MITOGEN ACTIVATED PROTEIN 6 (MPK6) and SPEECHLESS (SPCH) (Samakovli et al ., 2020b).…”

“…A fundamental prerequisite of a cell is to integrate external, internal or stress stimulus in regulatory network of genetic and protein interactions and to constantly respond by reshaping appropriate development and adaptation. The interaction of HSP90 with kinases, transcription factors or brassinosteroid signaling components is dynamically affecting genetic circuitries leading to various developmental processes (Samakovli et al ., 2007, 2014; Lachowiec et al ., 2013; Shigeta et al ., 2015; Margaritopoulou et al ., 2016; Wang et al ., 2016; Watanabe et al ., 2016; Samakovli et al ., 2020a,b; Tichá et al ., 2020). In brassinosteroid signaling, HSP90 interacts and influences BIN2 and BES1 complex localization while HSP90 nuclear localization is influenced by brassinolide (BL; Samakovli et al ., 2014, 2020a).…”