Auxin stimulates S6 ribosomal protein phosphorylation in maize thereby affecting protein synthesis regulation

Abstract

Auxin is known to stimulate protein synthesis in many plant tissues, but the mechanisms involved in this process are unknown. The present research inquires whether auxin might regulate selective translation of mRNAs by inducing S6 ribosomal protein phosphorylation on the 40S ribosomal subunit in maize (Zea mays L.). Maize embryonic axes auxin-stimulated by natural (IAA) or synthetic (Dicamba or 1-NAA) auxins, selectively increased ribosomal protein synthesis. This effect was not reproduced by auxin inactive analogue 2-NAA. Enhanced S6 ribosomal protein phosphorylation on the 40S ribosomal subunit was also observed after auxin stimulation, as measured by [32P] incorporation into this protein. This increment did not occur when stimulation was performed with the inactive auxin analogue. Further, increased recruitment into polysomes of two 5'TOP-like mRNAs, encoding for the initiation translation factor eIF-iso4E and the S6 ribosomal protein, was also found after auxin stimulation of maize axes. A positive correlation was established between the levels of S6 ribosomal protein phosphorylation and the S6 ribosomal protein transcript recruitment into polysomes by means of okadaic acid or heat shock application to maize axes. These data indicate that auxin stimulates S6 ribosomal protein phosphorylation on maize ribosomes, concomitant to the recruitment of specific mRNAs (5'TOP-like mRNAs) into polysomes for translation. It is proposed that by this mechanism auxin regulate the synthesis of specific proteins in maize tissues.

The Arabidopsis TOR Kinase Specifically Regulates the Expression of Nuclear Genes Coding for Plastidic Ribosomal Proteins and the Phosphorylation of the Cytosolic Ribosomal Protein S6

“…It is thus tempting to hypothesize that TOR has been recruited in plants to regulate specifically in leaves the translation of nuclear mRNAs coding for chloroplastic ribosomal proteins. It was previously shown that translation of animal TOP-containing mRNAs can be differentially regulated in vitro in a wheat germ extract (Shama and Meyuhas, 1996) and that auxin stimulates S6 ribosomal protein phosphorylation on maize ribosomes and the recruitment of TOP-like mRNAs for translation (Beltrán-Peña et al, 2002). Since TOR is also activated by auxin (Schepetilnikov et al, 2013) these data suggest that plant mRNAs containing TOP-related motifs could also be regulated in a TOR- and phosphorylated S6-dependent manner.…”

Mechanism of Cytoplasmic mRNA Translation

“…In Arabidopsis, RPS6 phosphorylation is promoted during the day (Turkina et al, 2011;Boex-Fontvieille et al, 2013) and in response to auxin and cytokinin (Turck et al, 2004), but is repressed by hypoxia . In monocots, RPS6 is phosphorylated in embryos during germination (Beltrán-Peña et al, 2002) and its phosphorylation rapidly declines following hypoxia, heat shock and singlet oxygen treatment (Williams et al, 2003;Khandal et al, 2009). The RPS6 kinase of Arabidopsis, AtS6K1, is important in regulating cell division and growth (Henriques et al, 2010;Shin et al, 2012).…”

Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors

“…Several ribosomal proteins have been associated with auxin-related developmental processes, such as cell proliferation, cell expansion, and polarity establishment in leaves (39)(40)(41). Auxins also trigger the coordinate expression of ribosomal protein mRNAs (55,56), increase de novo ribosomal protein synthesis (57), and change ribosomal protein phosphorylation patterns (58,59). In our study, mutations in multiple ribosomal genes caused specific auxin-related defects rather than a nonspecific defect in translation.…”