Rice cyclophilin OsCYP18‐2 is translocated to the nucleus by an interaction with SKIP and enhances drought tolerance in rice andArabidopsis

Abstract

Cyclophilin 18-2 (CYP18-2) genes, homologues of human peptidyl-prolyl isomerase-like 1 (PPiL1), are conserved across multicellular organisms and Schizosaccharomyces pombe. Although PPiL1 is known to interact with ski-interacting protein (SKIP), a transcriptional co-regulator and spliceosomal component, there have been no functional analyses of PPiL1 homologues in plants. Rice cyclophilin 18-2 (OsCYP18-2) bound directly to amino acids 56-95 of OsSKIP and its binding was independent of cyclosporin A, a cyclophilin-binding drug. Moreover, OsCYP18-2 exhibited PPIase activity regardless of its interaction with OsSKIP. Therefore, the binding site for OsCYP18-2's interaction with SKIP was distinct from the PPIase active site. OsCYP18-2's interaction with SKIP full-length protein enabled OsCYP18-2's translocation from the cytoplasm into the nucleus and AtSKIP interacted in planta with both AtCYP18-2 and OsCYP18-2. Drought and salt stress induced similar expression of OsCYP18-2 and OsSKIP. Overexpression of OsCYP18-2 in transgenic rice and Arabidopsis thaliana plants enhanced drought tolerance and altered expression and pre-mRNA splicing patterns of stress-related genes in Arabidopsis under drought conditions. Furthermore, OsCYP18-2 caused transcriptional activation with/without OsSKIP in the GAL4 system of yeast; thus the OsSKIP-OsCYP18-2 interaction has an important role in the transcriptional and post-transcriptional regulation of stress-related genes and increases tolerance to drought stress.

Bioinformatic and expression analysis of the Brassica napus L. cyclophilins

“…One example is BnCYP18-1 which is the only B. napus homolog of AtCYP18-2 with a full length CLD (with 95% sequence identity, Table 2). It has been shown that the Arabidopsis CYP AtCYP18-2 is recruited by AtSKIP to the nucleus to regulate pre-mRNA splicing 55 . Because of the high homology, the oilseed rape variant might fulfil a similar role in the nucleus of B. napus cells.…”

Discovery of MicroRNAs and Their Target Genes Related to Drought in Paulownia “Yuza 1” by High-Throughput Sequencing

“…Cytochromes (CYPs) are immunophilins, and several CYP family members had been discovered in model plants such as A. thaliana , Oryza sativa , P. trichocarpa , Morus notabilis , and Carica papaya [37–41]. In rice, OsCYP20-2 was shown to take part in the abiotic stress response, and overexpression of OsCYP18-2 by interacting with ski-interacting protein (SKIP) can enhance drought tolerance in rice and Arabidopsis [42]. Additionally, SKIP was also found to participate in splicing precursor mRNA in Arabidopsis [43], and the cis - and trans -isomerase peptidyl-prolyl isomerase-like 1 is recruited by SKIP into the spliceosome where precursor mRNA splicing occurs [44], suggesting that overexpression of OsCYP18-2 affected the expression of alternative splicing variants of stress-related genes by SKIP under drought condition [42].…”

“…In rice, OsCYP20-2 was shown to take part in the abiotic stress response, and overexpression of OsCYP18-2 by interacting with ski-interacting protein (SKIP) can enhance drought tolerance in rice and Arabidopsis [42]. Additionally, SKIP was also found to participate in splicing precursor mRNA in Arabidopsis [43], and the cis - and trans -isomerase peptidyl-prolyl isomerase-like 1 is recruited by SKIP into the spliceosome where precursor mRNA splicing occurs [44], suggesting that overexpression of OsCYP18-2 affected the expression of alternative splicing variants of stress-related genes by SKIP under drought condition [42]. Cyclophilin is suggested to be an unspecific stress-responsive protein in plants and plays a role in the defense response, and it was upregulated in potato and tobacco under stresses [45, 46].…”

Overexpression of Golgi Protein CYP21-4s Improves Crop Productivity in Potato and Rice by Increasing the Abundance of Mannosidic Glycoproteins

“…A company (Abfrontier, Seoul, Korea) carried out peptide synthesis, immunization, and antiserum purification. Immunoblot analysis was performed as described previously (Lee et al, 2015b). The prepared polyclonal CYP21-4 antibody was hybridized with total potato and rice proteins from the leaf tissue, and the CYP21-4 protein bands were confirmed as having the predicted size (determined from the mobility of recombinant OsCYP21-4 protein).…”

“…The representative model plants, Arabidopsis and rice have established classification systems for the immunophilin family of receptors (He et al, 2004; Ahn et al, 2010). Previously, we classified rice immunophilins, including 29 OsFKBPs and 26 OsCYPs (Ahn et al, 2010), and used reverse genetics to identify stress-responsive rice CYPs involved in salt, drought, photosynthetic, and cold stress (Park et al, 2013; Seok et al, 2014; Lee et al, 2015a,b, 2016; Yoon et al, 2016). In addition, rice CYP21-4 (OsCYP21-4) was identified as an unusual Golgi-localized immunophilin that contributes to oxidative stress tolerance by regulating peroxidase activity (Lee et al, 2015a).…”