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Changes at the 3′-untranslated region stabilize Rubisco activase transcript levels during heat stress in Arabidopsis

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Abstract

Inhibition of photosynthesis by heat stress is accompanied by functional impairment of Rubisco’s chaperone, activase (RCA), resulting in deactivation of Rubisco. Since activase is extremely sensitive to thermal denaturation, changes in expression of RCA at the transcript or protein level could provide a mechanism for acclimation of photosynthesis to prolonged heat stress. Using quantitative real-time PCR (qPCR) we show steady-state RCA transcript levels in Arabidopsis thaliana are stabilized during prolonged exposure to moderate heat (35  °C). A survey of RCA transcripts indicates heat stress did not alter the relative abundance of transcripts encoding α and β-isoforms of activase that are produced by alternative splicing of the pre-mRNA. Instead, mRNA stabilization in heat-stressed plants coincided with a significant reduction in the average length of activase 3′-untranslated regions, and was associated with enrichment of an uncharacterized activase mRNA splice variant, AtRCAβ2. Transcript-specific qPCR revealed AtRCAβ2 mRNA was more stable than AtRCAα and AtRCAβ mRNA in heat-stressed plants. Using an inducible transgenic system, we found that RCA transcripts lacking their native 3′-untranslated region were significantly more stable than their full-length counterparts in vivo. Using this system, stability of the RCA protein was examined over 24 h in vivo, in the absence of RCA transcription. At both optimal and elevated temperatures, RCA protein levels remained stable in plants lacking RCA mRNA, but increased when RCA mRNA was present, particularly in heat-stressed plants. This study reveals a possible mechanism, involving post-transcriptional regulation of an important photosynthesis regulatory gene, for acclimation of photosynthesis to heat stress.

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Acknowledgments

We thank Dr. Michael E. Salvucci for critical review of this manuscript, and for providing plasmid containing full-length cDNA encoding AtRCAβ. We thank Dr. Peter B. Goldsbrough for providing Agrobacterium strain GV3850 for plant transformation. This work was supported by grants from the National Science Foundation to B.P.D. (NSF-RUI Molecular and Cellular Biosciences grant no. 0820877 and NSF-MRI grant no. 0820756) and by a Grinnell College Harris Faculty Fellowship to B.P.D. We also acknowledge institutional support from Grinnell College’s Committee for the Support of Faculty Scholarship.

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  1. Department of Biology, Grinnell College, 1116 8th Avenue, Grinnell, IA, 50112, USA

    Benjamin P. DeRidder, Mikel E. Shybut, Michael C. Dyle, Karl A. G. Kremling & Mariya B. Shapiro

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DeRidder, B.P., Shybut, M.E., Dyle, M.C. et al. Changes at the 3′-untranslated region stabilize Rubisco activase transcript levels during heat stress in Arabidopsis. Planta 236, 463–476 (2012). https://doi.org/10.1007/s00425-012-1623-0

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