May 2, 2014

Review: A Chloroplast Retrograde Signal Regulates Nuclear Alternative Splicing

in Science 25 April 2014: Vol. 344 no. 6182 pp. 427-430 DOI: 10.1126/science.1250322 

(click here to download the original article)

 Ezequiel Petrillo1, Micaela A. Godoy Herz1, Armin Fuchs2, Dominik Reifer2, John Fuller3, Marcelo J. Yanovsky4, Craig Simpson3, John W. S. Brown3,5, Andrea Barta2, Maria Kalyna2, Alberto R. Kornblihtt1,*

* Corresponding author (
1Laboratorio de Fisiología y Biología Molecular, Departamento de Fisiología, Biología Molecular y Celular, IFIBYNE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, C1428EHA Buenos Aires, Argentina.
2Max F. Perutz Laboratories, Medical University of Vienna, A-1030 Vienna, Austria.
3Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, Dundee, Scotland.
4Fundación Instituto Leloir, IIBBA-CONICET, C1405BWE Buenos Aires, Argentina.
5Division of Plant Sciences, University of Dundee at The James Hutton Institute, Invergowrie, Dundee, Scotland.

            The role of light again features prominently in this week’s report at the Plant Biology Review. We recently saw how light rapidly induces the transcription of the AP2/ERF transcription factor family in Arabidopsis, a process involving retrograde signaling from the chloroplast. Vogel et al. (2014) demonstrated the involvement of triose phosphates as the metabolite signal key to activating transcript on this short time scale when plants were moved from darkness to light conditions, a process leading to transcript level changes on the scale of minutes.Another report on chloroplast retrograde signaling mediated by light is reviewed here today, this time published in Science by the group of Alberto Kornblihtt from the Laboratorio de Fisiología y Biología Molecular at the University of Buenos Aires, Argentina.
           Petrillo et al. (2014) describe as an of yet unknown signal which not only mediates alternative splicing of specific genes, but also travels from leaves, where it is originated to roots, where it exerts the same effect. This effect involves alternative splicing of genes such At-RS31, a Ser-Arg rich splicing factor. Fully spliced transcripts of this gene (mRNA1) encode the full length, functional protein whereas the alternative splice forms (mRNAs 2 and 3) remain almost exclusively in the nucleus. Therefore, alternative splicing of the At-RS31 gene is a form of post-transcriptional downregulation. That a gene involved in splicing is itself subject to regulation via alternative splicing is a common motif in biology which might be denoted meta-regulation. In this case, At-RS31 alternative splice forms become more abundant than the functional mRNA1 form when the plant is kept in the dark for long periods, effectively reducing its activity under low light conditions. The authors measured this phenomenon by calculating its splicing index (SI), defined as the ratio of the longest splice form divided by the sum of all splice forms. Therefore, a SI close to one suggests mostly alternative forms of the transcript which are presumably non-functional, and in the case of At-RS31 this occurs only when plants are kept in darkness or low light for extended periods.
Returning plants to light abruptly abolishes this effect and quickly returned the SI to low levels (< 0.2), meaning a high proportion of the mRNA1 form, but it took at least 24 hours of darkness for the SI of At-RS32 to increase significantly above light controls. Light intensity was also shown to affect At-RS32 splicing, with high light intensity resulting in lower SIs, and both blue and red light were equally effective at decreasing lowering its SI. When plants were transformed with the mRNA1 cDNA for At-RS31 so that splicing was not possible and transferred to darkness or low light conditions, they developed a palid phenotype, suggesting that At-RS31 downregulation is necessary for properly adjusting to darkness.
Narrowing down the metabolite signal proved more difficult, but by dissecting roots and shoots, they authors demonstrated that the signal originates in the leaves and travels to roots, where it has a similar effect on suppressing alternative splice forms of At-RS31 (decreasing SI). Generation of this chloroplast signal occurs between photosystems (PS) I and II and requires reduced plastoquinone, which the authors demonstrated using an elegant experimental design of electron transfer inhibitors for PSI and PSII. A reprised role for sucrose in breaking bud dormancy was recently reviewed here, and triose phosphates were implicated as chloroplast retrograde signals in the activation of AP2/ERF transcription factors (Vogel et al 2014). However, Petrillo et al. have ruled out sugars and sugar signaling pathways as the active signal affecting alternative splicing, and while their evidence suggests plastoquinone mediates initiation of a signal  originating in the chloroplasts and traveling throughout the plant, the precise identity of the signal itself remains unknown at this time.

Petrillo, E., Godoy Herz, M.A., Fuchs, A., Reifer, D., Fuller, J., Yanovsky, M.J., Simpson, C., Brown, J.W.S., Barta, A., Kalyna, M., and Kornblihtt, A.R. (2014). A chloroplast retrograde signal regulates nuclear alternative splicing. Science 344, 427-430.
Vogel, M.O., Moore, M., König, K., Pecher, P., Alsharafa, K., Lee, J., and Dietz, K.-J. (2014). Fast retrograde signaling in response to high light Involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell.

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