Plant Signaling & Behavior 7:9, 1056-1057; September 2012; © 2012 Landes Bioscience
Oscillation regulation of Ca2+/calmodulin and heat-stress related genes in response to heat stress in rice (Oryza sativa L.) Hui-Chen Wu† and Tsung-Luo Jinn*
†
Current affiliation: Institut de Recherche pour le Développement (IRD); Montpellier Cedex 5, France
Keywords: Ca 2+, calmodulin, heat shock signaling, temporal–spatial regulation, thermotolerance
The Ca2+/calmodulin (CaM) signaling pathway mediates the heat stress (HS) response and acquisition of thermotolerance in plants. We showed that the rice CaM1-1 isoform can interpret a Ca2+ signature difference in amplitude, frequency, and temporal–spatial properties in regulating transcription of nucleoplasmic small heat-shock protein gene (sHSPC/N) during HS. Ca2+ and A23187 treatments under HS generated an intense and sustained increase in [Ca2+]cyt and accelerated the expression of CaM1-1 and sHSPC/N genes, which suggests that HS-induced apoplastic Ca2+ influx was responsible for the [Ca2+]cyt transient and downstream HS signaling. Here, we discuss an emerging paradigm in the oscillation regulation of CaM1-1 expression during HS and highlight the areas that need further investigation.
Ca 2+ signaling has been long considered a crucial process in response to a wide range of stimuli from biotic and abiotic environmental stresses. Ca 2+ signals differing in amplitude, frequency, and temporal and spatial properties trigger different transcriptional responses.1 These responses are accomplished by downstream effectors such as calmodulin (CaM) to decode the Ca 2+ signals of differing origins and temporal-spatial properties. CaM as a primary sensor binds Ca 2+ and regulates the activity of a wide range of effectors by converting Ca 2+ signals into transcriptional responses, protein phosphorylation or metabolic changes. In previous studies, we showed that Ca 2+ could relieve an EGTA effect, chelating the intrinsic removable Ca 2+ from the cell wall liberated by HS, to rescue the acquisition of thermotolerance.2,3 Our recent studies demonstrated that the HS-induced [Ca 2+] cyt transient had monophasic and biphasic shapes in different tissues of rice and that the CaM1-1 isoform was an important component of the HS signal transduction pathway.4 Ca 2+ entry across the plasma membrane is essential for heat to induce HS-related gene transcription in a strict Ca 2+ -dependent manner.5 Remarkably, we found that Ca 2+ treatment at normal growth temperature could not mimic the HS-induced Ca 2+ signature. Conversely, Ca 2+ and A23187 treatments under HS accelerated both the amplitude and frequency of the [Ca 2+] cyt transient. The corresponding result was shown in Arabidopsis (Fig. 1). These observations in different plants led us to suggest that the HS-triggered [Ca 2+] cyt transient could be physiologically adjusted depending on the intensity of the HS signal.
We found the transcript level of CaM1-1 and sHSPC/N tightly linked with that of the [Ca 2+] cyt transient during HS.4 The oscillation of the [Ca 2+] cyt transient, “enabling signature,” was decoded by CaM1-1 to transmit the HS signal for inducing sHSPC/N transcription. Ca 2+ and A23187 treatments strengthened and accelerated the [Ca 2+] cyt transient and quickly induced CaM1-1 and sHSPC/N transcription under HS. Therefore, CaM1-1 interprets the Ca 2+ signature by the cytosolic Ca 2+ concentration and by temporal-spatial Ca 2+ parameters. These data raise the question of why the transcript level of CaM1-1 shows an up-and-down oscillating profile in response to HS. We suggest that the central decoder CaM1-1 may be negatively or positively cross regulated by different CaM isoforms (co-decoders) to complete the HS signaling pathway. Here, we summarize the role of CaM1-1 as a central decoder that can be regulated by other codecoders to perceive [Ca 2+] cyt oscillations in level involved in HS signaling (Fig. 2). However, the detailed mechanism remains to be elucidated. Recently, microRNAs (miRNAs) were found to be crucial in regulating gene expression, development, metabolism and stress responses.6,7 We found that the promoter and/or untranslated region of CaM genes had differential miRNAs target sites, which suggests that CaM genes may be regulated by miRNAs at the posttranscriptional level. Interestingly, CaM1-1 shows miR168a and miR408 target sites, and both miRNAs harbor HS-responsive cismotifs, the HS elements (HSE),8 which may regulate transcription of these miRNAs in response to HS. Notably, miR168a and miR408 regulate their target genes by degradation and changing
*Correspondence to: Tsung-Luo Jinn; Email:
[email protected] Submitted: 06/03/12; Revised: 06/13/12; Accepted: 06/13/12 http://dx.doi.org/10.4161/psb.21124 1056
Plant Signaling & Behavior
Volume 7 Issue 9
©2012 Landes Bioscience. Do not distribute.
Institute of Plant Biology and Department of Life Science; National Taiwan University; Taipei, Taiwan
Figure 1. Heat shock-triggered [Ca2+]cyt transient in Arabidopsis. Root tips of 3-d-old Arabidopsis seedlings were pretreated with 1 μM Fluo-3/ AM (for Ca2+ fluorescence intensity examined by laser scanning confocal microscopy), then treated with 10 mM CaCl2 or 50 μM A23187 at 26°C (control) or 37°C (HS) as described (Wu et al. 2012). H2O treatment was a reference. Fluorescence intensity was measured by scanning 10 to 20 cells per assay in four independent replicates, which all showed similar profiles.
their abundance.8 The expression of some miRNAs shows oscillating profiles in Arabidopsis;9 a similar mechanism in rice may explain the oscillating patterns of CaM1-1 expression. Disclosure of Potential Conflicts of Interest
Figure 2. The hypothetical model of molecular mechanism implicated in the heat shock-triggered Ca2+ signatures are interpret by CaM1-1 and may require co-decoder for transcription of sHSPC/N. Ca2+ or A23187 treatment under heat shock triggered [Ca2+]cyt transient with different kinetics. The signal-specific Ca2+ signature, “enabling signal,” is interpreted by the central decoder CaM1-1 and activates the downstream sHSPC/N gene induction. Another co-decoder component may help or repress CaM1-1 function during HS signaling.
Acknowledgments
Support for this work is from National Taiwan University (10R80917-3) and partially by the National Science Council, Taiwan (98-2311-B-002-007-MY3) to T.-L. J.
No potential conflicts of interest were disclosed. References 1.
Chawla S, Bading H. CREB/CBP and SRE-interacting transcriptional regulators are fast on-off switches: duration of calcium transients specifies the magnitude of transcriptional responses. J Neurochem 2001; 79:84958; PMID:11723177; http://dx.doi.org/10.1046/ j.1471-4159.2001.00645.x. 2. Wu HC, Hsu SF, Luo DL, Chen SJ, Huang WD, Lur HS, et al. Recovery of heat shock-triggered released apoplastic Ca2+ accompanied by pectin methylesterase activity is required for thermotolerance in soybean seedlings. J Exp Bot 2010; 61:2843-52; PMID:20444907; http://dx.doi.org/10.1093/jxb/erq121. 3. Wu HC, Jinn TL. Heat shock-triggered Ca2+ mobilization accompanied by pectin methylesterase activity and cytosolic Ca2+ oscillation are crucial for plant thermotolerance. Plant Signal Behav 2010; 5:12526; PMID:20948293; http://dx.doi.org/10.4161/ psb.5.10.12607.
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4. Wu HC, Luo DL, Vignols F, Jinn TL. Heat shockinduced biphasic Ca(2+) signature and OsCaM1-1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.). Plant Cell Environ 2012; PMID:22428987; http:// dx.doi.org/10.1111/j.1365-3040.2012.02508.x, In press. 5. Horváth I, Glatz A, Nakamoto H, Mishkind ML, Munnik T, Saidi Y, et al. Heat shock response in photosynthetic organisms: Membrane and lipid connections. Prog Lipid Res 2012; 51:208-20; PMID:22484828; http://dx.doi.org/10.1016/j.plipres.2012.02.002. 6. Baulcombe D. RNA silencing in plants. Nature 2004; 431:356-63; PMID:15372043; http://dx.doi. org/10.1038/nature02874.
Plant Signaling & Behavior
7.
Vaucheret H, Mallory AC, Bartel DP. AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 2006; 22:129-36; PMID:16600876; http:// dx.doi.org/10.1016/j.molcel.2006.03.011. 8. Jia X, Ren L, Chen QJ, Li R, Tang G. UV-Bresponsive microRNAs in Populus tremula. J Plant Physiol 2009; 166:2046-57; PMID:19628301; http:// dx.doi.org/10.1016/j.jplph.2009.06.011. 9. Siré C, MorenoAB, Garcia-Chapa M, López-Moya JJ, San Segundo B. Diurnal oscillation in the accumulation of Arabidopsis microRNAs, miR167, miR168, miR171 and miR398. FEBS Lett 2009; 583:1039-44; PMID:19236868; http://dx.doi.org/10.1016/j.febslet.2009.02.024.
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