Arabidopsis HSP90 protein modulates RPP4‐mediated temperature‐dependent cell death and defense responses

Abstract

SummaryPlant defense responses are regulated by temperature. In Arabidopsis, the chilling-sensitive mutant chs2-1 (rpp4-1d) contains a gain-of-function mutation in the TIR-NB-LRR (Toll and interleukin 1 receptor-nucleotide binding-leucine-rich repeat) gene, RPP4 (RECOGNITION OF PERONOSPORA PARASITICA 4), which leads to constitutive activation of the defense response at low temperatures.Here, we identified and characterized two suppressors of rpp4-1d from a genetic screen, hsp90.2 and hsp90.3, which carry point mutations in the cytosolic heat shock proteins HSP90.2 and HSP90.3, respectively.The hsp90 mutants suppressed the chilling sensitivity of rpp4-1d, including seedling lethality, activation of the defense responses and cell death under chilling stress. The hsp90 mutants exhibited compromised RPM1 (RESISTANCE TO PSEUDOMONAS MACULICOLA 1)-, RPS4 (RESISTANCE TO P. SYRINGAE 4)-and RPP4-mediated pathogen resistance. The wild-type RPP4 and the mutated form rpp4 could interact with HSP90 to form a protein complex. Furthermore, RPP4 and rpp4 proteins accumulated in the cytoplasm and nucleus at normal temperatures, whereas the nuclear accumulation of the mutated rpp4 was decreased at low temperatures. Genetic analysis of the intragenic suppressors of rpp4-1d revealed the important functions of the NB-ARC and LRR domains of RPP4 in temperature-dependent defense signaling. In addition, the rpp4-1d-induced chilling sensitivity was largely independent of the WRKY70 or MOS (modifier of snc1) genes. [Correction added after online publication 11 March 2013: the expansions of TIR-NB-LRR and RPS4 were amended] This study reveals that Arabidopsis HSP90 regulates RPP4-mediated temperature-dependent cell death and defense responses.

The heat‐shock protein/chaperone network and multiple stress resistance

“…This complex is regulating important R proteins like RPM1 (resistance to Pseudomonas maculicola 1), RPS2, RPS4 (resistance to Pseudomonas syringae 2 and 4), RPP4 (recognition of Peronospora parasitica 4 (Bao et al . () Hubert et al . (); Takahashi et al .…”

The plant hypersensitive response: concepts, control and consequences

“…This phenomenon is also commonly observed for auto‐active NLRs (Heidrich et al , ; Negeri et al , ; discussed more below) and in hybrid necrosis controlled by NLRs (Bomblies et al , ; also discussed below; Muralidharan et al , ). In some cases chilling sensitive phenotypes, where leaf yellowing and cell death are observed at temperatures under 16 °C, were shown to be caused by mutated versions of NLRs (Bao et al , ; Huang et al , ).…”

“…In most examples of temperature‐sensitive HR, NLR protein levels cannot be measured since the necessary antibodies are not available. However, the levels of the NLR rpp4 that conferred chilling sensitivity in Arabidopsis and of the autoactive NLR SNC1 were not altered by temperature (Bao et al , ; Zhu et al , ), indicating that mechanisms other than those affecting protein accumulation may be important for NLR temperature sensitivity.…”

The chaperone MeHSP90 recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava

“…AtHSP90 is also a chaperone for the auxin receptor transport inhibitor response 1 (TIR1) and buffers auxin‐responsive phenotypes (Wang et al , ; Watanabe et al , ). Except for mutant analysis, two protein inhibitors (geldanamycin (GDA) and radicicol (RAD)) are also widely used to reveal the functions of HSP90s in plants (Baro et al , ; Queitsch et al , ; Samakovli et al , ; Wang et al , ; Watanabe et al , ). So far, the HSP90 gene family has been reported on a genome‐wide basis in several plant species, including Arabidopsis (Krishna & Gloor, ), Populus trichocarpa (Zhang et al , ), tomato (Zai et al , ), chickpea and pigeonpea (Agarwal et al , ), foxtail millet (Singh et al , ), and Brachypodium distachyon (Zhang et al , ).…”